Department of Neurobiology, Northeastern Ohio Universities College of Medicine, Rootstown, Ohio 44272-0095
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ABSTRACT |
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Wenstrup, Jeffrey J.. Frequency Organization and Responses to Complex Sounds in the Medial Geniculate Body of the Mustached Bat. J. Neurophysiol. 82: 2528-2544, 1999. The auditory cortex of the mustached bat (Pteronotus parnellii) displays some of the most highly developed physiological and organizational features described in mammalian auditory cortex. This study examines response properties and organization in the medial geniculate body (MGB) that may contribute to these features of auditory cortex. About 25% of 427 auditory responses had simple frequency tuning with single excitatory tuning curves. The remainder displayed more complex frequency tuning using two-tone or noise stimuli. Most of these were combination-sensitive, responsive to combinations of different frequency bands within sonar or social vocalizations. They included FM-FM neurons, responsive to different harmonic elements of the frequency modulated (FM) sweep in the sonar signal, and H1-CF neurons, responsive to combinations of the bat's first sonar harmonic (H1) and a higher harmonic of the constant frequency (CF) sonar signal. Most combination-sensitive neurons (86%) showed facilitatory interactions. Neurons tuned to frequencies outside the biosonar range also displayed combination-sensitive responses, perhaps related to analyses of social vocalizations. Complex spectral responses were distributed throughout dorsal and ventral divisions of the MGB, forming a major feature of this bat's analysis of complex sounds. The auditory sector of the thalamic reticular nucleus also was dominated by complex spectral responses to sounds. The ventral division was organized tonotopically, based on best frequencies of singly tuned neurons and higher best frequencies of combination-sensitive neurons. Best frequencies were lowest ventrolaterally, increasing dorsally and then ventromedially. However, representations of frequencies associated with higher harmonics of the FM sonar signal were reduced greatly. Frequency organization in the dorsal division was not tonotopic; within the middle one-third of MGB, combination-sensitive responses to second and third harmonic CF sonar signals (60-63 and 90-94 kHz) occurred in adjacent regions. In the rostral one-third, combination-sensitive responses to second, third, and fourth harmonic FM frequency bands predominated. These FM-FM neurons, thought to be selective for delay between an emitted pulse and echo, showed some organization of delay selectivity. The organization of frequency sensitivity in the MGB suggests a major rewiring of the output of the central nucleus of the inferior colliculus, by which collicular neurons tuned to the bat's FM sonar signals mostly project to the dorsal, not the ventral, division. Because physiological differences between collicular and MGB neurons are minor, a major role of the tecto-thalamic projection in the mustached bat may be the reorganization of responses to provide for cortical representations of sonar target features.
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INTRODUCTION |
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The auditory cortex of the mustached bat
(Pteronotus parnellii) displays some of the most highly
developed features described in mammalian auditory cortex. Many of
these features are based on a fundamental neuronal response property
called combination sensitivity, characterized by neural integration of
inputs from distinct frequency bands in the bat's audible range
(Suga et al. 1978, 1983
). The neural comparisons
facilitate the analysis of spectrally and temporally complex
vocalizations. Although these properties occur in the forebrains of
many vertebrates, from frogs to birds to primates (Fuzessery and
Feng 1983
; Margoliash and Fortune 1992
;
Rauschecker 1997
), their physiological and
organizational features have been described best in the mustached bat
(Fitzpatrick et al. 1998b
; Ohlemiller et al.
1996
; O'Neill and Suga 1982
; Suga et al.
1983
). The focus of this paper is on physiological and organizational properties in the medial geniculate body (MGB) that may
contribute to this specialized auditory cortex.
The mustached bat displays two highly developed acoustic
behaviorsbiosonar and social communication
that may rely on
specialized, combination-sensitive responses of auditory cortical
neurons. In sonar behavior, the mustached bat is believed to use
combination-sensitive responses to its multiharmonic sonar call (Fig.
1) to extract information about a
target's distance and movement. The mapping of sonar-related response
properties across subregions of auditory cortex represents one of the
most extensive studies of behaviorally relevant functional organization
in mammalian auditory cortex (Fitzpatrick et al. 1998b
;
O'Neill and Suga 1982
; Suga and O'Neill 1979
; Suga et al. 1983
). The mustached bat's
highly developed acoustic communication (Kanwal et al.
1994
) also uses combination-sensitive responses. Neurons in
auditory cortex appear to respond selectively to certain combinations
within or between syllables (Esser et al. 1997
;
Ohlemiller et al. 1996
). The types and organization of
such combination-sensitive responses provides insight to the species-specific processing of complex sounds in auditory cortex.
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Because distinct frequency bands used in sonar or social communication
signals may provide different information to a bat, the neural analyses
and representations of these frequency bands may likewise differ. One
example concerns frequency bands associated with the mustached bat's
analysis of the distance of objects using sonar. These bands correspond
to the harmonics of the frequency modulated (FM) downsweep in the
bat's sonar signal (Fig. 1). In auditory cortex, neurons sensitive to
combinations of FM signals display physiological properties and
organization that are not shared by neurons tuned to the constant
frequency (CF) component in sonar signals or by neurons tuned to
frequencies outside the sonar bands (Fitzpatrick et al.
1998b; Suga et al. 1983
). One physiological
property of the neurons responding to FM bands is delay tuning, which
can be related to the bat's analysis of target distance in
echolocation (O'Neill and Suga 1982
; Suga and
O'Neill 1979
). Neurons tuned to the FM frequency bands are
virtually absent from the main tonotopic axis of primary auditory
cortex but are instead located in other cortical areas and appear to be
organized according to delay tuning (Fitzpatrick et al.
1998b
; O'Neill and Suga 1982
; Suga and
Horikawa 1986
). Although these neurons also may analyze social
communication signals or other sounds, their responses and organization
appear strongly related to the analysis of sonar echoes. Thus a key to
understanding auditory cortical or thalamic organization is an
understanding of how information within specific frequency bands is
analyzed and represented. This study focuses on the representation and
physiological properties in the auditory thalamus of nine frequency
bands defined by their inclusion in sonar and social vocalizations
(Fig. 1).
Combination-sensitive responses require temporally sensitive neural
integration of inputs having distinct frequency receptive fields, in
much the same way that visual motion-selective cells require temporally
sensitive integration of inputs with distinct spatial receptive fields
(Albright and Stoner 1995; Newsome and Salzman
1993
). The site(s) and features of this integration in the
auditory system are not certain, but they clearly occur at levels of
the ascending auditory pathway below the MGB (Mittmann and
Wenstrup 1995
; Portfors and Wenstrup 1999b
;
Wenstrup and Grose 1995
; Yan and Suga
1996
), perhaps in the inferior colliculus (Leroy and
Wenstrup 1999
; Wenstrup et al. 1999
). How then does the
MGB contribute to the physiology and organization of
combination-sensitive neurons in auditory cortex? This study addresses
that question by examining the types of combination-sensitive responses
in the MGB and thalamic reticular nucleus and their organization within the MGB.
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METHODS |
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Acoustic responses and their topographic distribution were
examined in the auditory thalamus of 21 greater mustached bats (Pteronotus parnellii parnellii) captured in Jamaica, West
Indies. Anatomic data from some experiments were reported elsewhere
(Wenstrup and Grose 1995). All animal procedures were
approved by the Institutional Animal Care and Use Committee.
Surgical procedures
The dorsal surface of the cerebral cortex was exposed in bats anesthetized with methoxyflurane (Metofane, Pitman-Moore, Inc., Mundelein, IL) in combination with pentobarbital sodium (5 mg/kg ip; Nembutal, Abbott Laboratories, North Chicago, IL) and acepromazine (2 mg/kg ip; Med-Tech, Buffalo, NY). A midline incision was made in the skin overlying the skull, and the muscles were reflected laterally. A tungsten ground electrode was cemented into the right cerebellar cortex, and a small hole (usually <0.5 mm) was placed in the skull over the cerebral cortex. A metal pin, cemented to the skull and secured to a restraining apparatus, maintained the head in a uniform position during physiological experiments. After application of a local anesthetic (lidocaine, Elkins-Sinns, Cherry Hill, NJ) and a topical antibiotic, the animal was placed in a holding cage to recover from the surgery.
Acoustic stimulation and recording
Beginning 1-2 days after surgery, physiological recordings were obtained from awake animals placed in a plexiglas restraining apparatus in a heated and humidified experimental chamber. Between electrode penetrations, the bat was offered water from a medicine dropper. Recording sessions generally lasted 4-6 h. The number of sessions for any bat ranged from one to seven.
Acoustic stimulation and data acquisition equipment have been described
in detail elsewhere (Portfors and Wenstrup 1999b; Wenstrup and Grose 1995
). Two different tone or noise
burst stimuli (3-30 ms duration, 1- or 0.5-ms rise-fall times, 3-4/s)
were separately generated, switched, and attenuated. The
digitally-generated sinusoids from the signal generators were accurate
to 1 Hz. Signals from the two channels were added, amplified, and sent
to a speaker placed 10 cm (30 cm in earlier experiments) away from the
bat and 25° into the sound field contralateral to the recording
electrode. The acoustic properties of the entire system were tested
using a calibrated microphone placed in the position normally occupied by the bat's head. There was a smooth, gradual decrease in the sound
pressure from 10 to 120 kHz of ~2.7 dB per 10 kHz. Distortion components in the speaker output were
60 dB below the sound level of
the signal, as measured by a fast Fourier analysis of the digitized microphone signal (1-MHz sampling rate).
The evoked activity of single unit and multiunit responses was recorded
with micropipettes having tip diameters of 5-10 µm (resistances of
1-15 M) and filled with a tracer to mark recording sites (described
later). Because tracers in most experiments were dissolved in 0.9%
saline, electrode resistance usually exceeded 10 M
. Electrodes were
advanced by a hydraulic micropositioner. Extracellular action
potentials were amplified, filtered (band-pass, 500-6000 Hz), and sent
through a window discriminator. The pulse output of the window
discriminator was digitized at 10 kHz. Peristimulus time (PST)
histograms, raster displays, and statistics on the neural responses
were generated by the computer. Multiunit responses that were analyzed
consisted of stimulus-locked clusters of clearly defined spikes; the
threshold of the window discriminator was adjusted to detect spike
activity exceeding the baseline level. The window discriminator output
also was displayed audiovisually.
Using a stereotaxic procedure as a guide, electrodes were placed to
record neural activity within the MGB or adjacent areas. Multiunit
responses usually were sampled at 100- to 150-µm intervals; single
units were examined whenever they could be isolated. Response properties were evaluated using tone or noise bursts. The best frequency (requiring the lowest intensity to elicit stimulus-locked spikes) and threshold at best frequency (the lowest intensity required
to elicit 1 spike to each of 5 consecutive stimuli) were measured. In
most cases, the Q10dB measure of tuning sharpness was obtained (best
frequency divided by the bandwidth 10 dB above threshold) because very
sharp tuning distinguishes MGB neurons analyzing some components of the
biosonar signal (Olsen and Suga 1991a
). Although
frequency tuning was measured to the nearest 0.1 or 0.01 kHz, Figs.
7-9 express tuning to the nearest kilohertz to save space. At some
recording sites, there was more than one peak in the excitatory tuning
curve. The threshold, best frequency, and usually the Q10dB value were
obtained for each excitatory tuning curve. Tone bursts were used
because nearly all sonar-related combination-sensitive MGB neurons are
reported to respond to these (Olsen and Suga 1991a
,b
).
Band-pass noise was used because some neurons tuned to frequency bands
outside the sonar range were found to respond preferentially to such stimuli.
Using a two-tone stimulus paradigm, neurons then were tested for
sensitivity to combinations of tones or noise bands across the bat's
audible range, including frequency bands used in sonar and
communication (Fig. 1). If a facilitatory or inhibitory interaction was
obtained, the frequencies, intensities, and timing of the two signals
were adjusted to obtain a strong combination-sensitive interaction.
Neurons were considered to be combination-sensitive if, for clearly
distinct frequency bands, the response to the two signals presented
together was 20% more (for facilitation) or 20% less (for inhibition)
than the sum of responses to the signals presented separately. The
degree of facilitation or inhibition was quantified as the index of
interaction (I), according to the following formula;
I = (Rc Rl
Rh)/ (Rc + Rl + Rh) where
Rc, Rl, and
Rh are, respectively, the neuron's
responses to the combination of the low- and high-frequency signals,
low-frequency signal alone, and high-frequency signal alone. An
interaction index value of 0.09 corresponds to 20% facilitation, the
criterion for combination-sensitive facilitation. Negative numbers
indicate combination-sensitive inhibition in which the excitatory
response to one signal is suppressed by the other signal. Interaction
index values of 1 and
1 indication maximum facilitation and
inhibition, respectively. If a combination-sensitive response was
observed, additional measures of frequency- and/or delay-dependent
facilitation (or inhibition) often were obtained.
One or two tracer deposits were used to mark electrode penetrations. At the end of a penetration, response properties again were characterized at tracer deposit sites. Iontophoretic deposits were made using a constant current source (Midgard model CS4).
Tracer and histological techniques
Tracers included wheat germ agglutinin conjugated to horseradish
peroxidase (Sigma Chemical, St. Louis, MO), biocytin (Sigma Chemical),
cholera toxin B-subunit (List Biologicals, Campbell, CA), Fluoro-Gold
(Fluorochrome, Englewood CO), or dextran-conjugated rhodamine and
fluorescein (Molecular Probes, Eugene, OR). Techniques used to deposit
and visualize the nonfluorescent tracers have been described in detail
elsewhere (Wenstrup and Grose 1995). Electrodes
containing fluorescent markers were filled with: 10% dextran-conjugated rhodamine or fluorescein in 0.9% NaCl, or 1% Fluoro-Gold in 0.1 M acetate buffer. Iontophoretic deposits used 5.0 µA (10 min, 7 s ON/7 s OFF) for the
dextran conjugates (positive current for rhodamine, negative current
for fluorescein) and +1.0 µA (5 min, 7 s ON/7 s
OFF) for Fluoro-Gold. Fluorescent labeling was viewed with
an Olympus BH-2 microscope and appropriate filter combinations.
After the last recording session, the animal was anesthetized deeply
with Nembutal (>60 mg/kg ip). Once nociceptive reflexes were
eliminated, the chest cavity was opened, and phosphate buffered saline
(pH 7.4) and an aldehyde fixative were perfused through the heart. The
fixed brain was blocked in the plane of the electrode penetrations,
inclined ~15° from dorsal and caudal to ventral and rostral,
consistent with previous anatomic and physiological studies of the MGB
(Wenstrup and Grose 1995; Wenstrup et al.
1994
). Each brain was refrigerated overnight in a 30%
sucrose-phosphate buffer solution before sectioning. Brains were
sectioned transversely on a freezing microtome at 30- to 40-µm
thickness, then collected into cold 0.1 M phosphate buffer or
phosphate-buffered saline. Every third section was processed by a
different protocol; one of the three series was stained with cresyl
violet. Cytoarchitectonic boundaries were drawn based on previous
descriptions (Wenstrup 1995
; Winer and Wenstrup
1994a
,b
).
To test qualitative observations regarding topographic organization of a response property (delay sensitivity), a nondirectional Pearson correlation analysis examined the relationship between best delay and recording site. Each recording site was plotted within the coordinates of the MGB in that animal. Caudorostral location was expressed relative to the caudal-to-rostral distance in that MGB, mediolateral location was expressed as the fraction of the maximal midline-to-lateral-edge distance of the MGB for that animal. Dorsoventral position was expressed relative to the ventralmost extension of the MGB, a reliable measure of dorsoventral position.
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RESULTS |
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This study is based on 551 physiological recording sites in the
MGB and surrounding regions. Sensitivity to complex sounds was examined
at 427 acoustically responsive recording sites. Because a major goal
was to map the distribution of basic response properties, both
single-unit and multiunit responses were included.
Combination-sensitive response properties in the MGB are clearly
observable in multiunit recordings (Wenstrup and Grose
1995). About 70% of the responses were multiunits, and similar
percentages were obtained for most subgroups of the population (Table
1). This finding supports the reliability
of multiunits for documenting most aspects of the complex responses
examined here.
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About one-quarter of the responses (112 of 427) had simple frequency tuning, with a single excitatory tuning curve (Table 1). These responses were tested for sensitivity to tone bursts outside their tuning curves, in which the frequency, amplitude, and relative timing of the second sound were varied. Additional tests were conducted with band-pass noise bursts. Although many of these responses could be inhibited by sounds on the flanks of the tuning curve or by lower frequency sounds at high sound levels, they were unaffected (neither facilitated or inhibited) by low-to-medium level sounds presented well outside their excitatory tuning curves.
Neurons with complex frequency tuning
The majority of auditory recording sites displayed complex responses to sound frequency (Table 1). These include multiple tuning, better sensitivity to noise than to tones, and combination-sensitive facilitation or inhibition as defined in the METHODS. Facilitatory combination-sensitive responses were the most common, comprising more than half of auditory responses tested for complex spectral sensitivity. Inhibitory combination-sensitive interactions, in which the excitatory response to a higher frequency signal was suppressed by a lower frequency signal, were uncommon in the auditory thalamus (<10% of auditory responses). As a group, the responses that showed multiple tuning or combination-sensitive inhibition responded well to single tone bursts within at least one frequency band. Among recording sites showing better sensitivity to noise or combination-sensitive facilitation, however, the responses to single tone bursts were weaker and more variable, never eliciting the maximum discharge.
Three major categories of combination-sensitive facilitation displayed
different functional properties and topographic distribution in the
MGB. The three categories are based partly on the frequency tuning of
the responses. In two categories, responses were to frequency ranges
used by specific components of the mustached bat's sonar signal (Fig.
1). In the third category, responses were to signals outside of the
sonar frequency range but within the range of acoustic signals used in
social communication (Kanwal et al. 1994) (Fig. 1). This
section describes distinguishing response properties of these
categories, including population measures of combination-sensitive
interactions that have been compared with similar data from neurons in
the inferior colliculus (Portfors and Wenstrup 1999b
).
FM-FM RESPONSES. These comprised 34% (n = 145) of all auditory responses. FM-FM neurons display temporally sensitive facilitation (or inhibition) that occurs when signals in two frequency bands are combined. One frequency band is associated with the first harmonic, FM sweep in the bat's sonar signal (FM1, 24-29 kHz), and the other associated with higher FM sweep harmonics (FM2, 48-59 kHz; FM3, 72-89 kHz; FM4, 96-119 kHz; Fig. 1). Figure 2A shows a facilitated FM-FM single unit, which responded weakly to a best frequency tone burst (74.8 kHz) or a lower frequency tone burst (27.6 kHz). It responded very strongly to combinations of the tone bursts but only when the higher frequency tone was delayed by 3-6 ms (Fig. 2A, delay tuning). The range of frequencies that evoked the facilitating effect (Fig. 2A, frequency tuning) corresponds to the FM1 and FM3 components of the bat's sonar signal.
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H1-CF RESPONSES. These responses (26% of acoustic responses) were sensitive to the combination of sounds in frequency ranges of the first sonar harmonic (H1, 24-31 kHz) and a higher harmonic of the CF sonar component in echoes (CF2, 60-63 kHz; CF3, 90-94 kHz). Figure 2B shows a facilitated H1-CF single unit. It responded weakly to a higher frequency tone burst (60.53 kHz) and even less to a lower frequency (26.2 kHz) tone burst (Fig. 2A, delay tuning). The neuron responded strongly to the combination of tone bursts when the higher frequency tone was present at times from 5 ms before to 5 ms after the lower frequency signal. The facilitating effect of the higher frequency signal had very sharp frequency tuning (Q10dB of 87), a characteristic of neurons tuned in the 60- to 63-kHz range throughout the mustached bat's auditory system (Fig. 2B, frequency tuning). In the presence of the facilitating 60.53 kHz signal, the neuron was broadly tuned to the FM1 frequency range (Q10dB of 6).
The higher frequency tuning of most H1-CF responses (86%) was to frequencies in the second harmonic CF signal, 60-63 kHz. For the lower frequency response, 83 of 85 H1-CF neurons showed low-frequency facilitation or inhibition tuned between 25.0 and 31.1 kHz (Fig. 3C). Eighty percent were in the 25.6- to 29.2-kHz range. This distribution is broader than for FM-FM neurons. It is noteworthy that the best low facilitative frequency for many H1-CF neurons was in the 27.5- to 28.5-kHz range (Fig. 3C), which served in other studies to distinguish the FM1 and CF1 frequency bands (Fitzpatrick et al. 1993NONSONAR COMBINATIONS. Other neurons showed facilitatory or inhibitory interactions between distinct spectral components in sounds. These also are called combination-sensitive, because their responses were in some ways similar to the FM-FM and H1-CF responses outlined in the preceding text. The single unit in Fig. 2C responded very weakly to single tone bursts but somewhat better to combinations of tones in the 12- to 23-kHz and 30- to 50-kHz range. Best frequencies were 23 and 41 kHz, respectively. There was strong facilitation (facilitation index of 0.64) between the two frequency inputs that occurred only at simultaneous presentation. However, the unit's overall response to combinations of tone bursts was not strong, remaining <1 spike/stimulus. Wideband noise (10-150 kHz) at the same attenuation setting yielded a response twice as strong.
The defining features of these responses were their tuning to sounds in the 10- to 23-kHz and 32- to 47-kHz ranges and the occurrence of the strongest combination-sensitive interactions when the two signals were presented simultaneously. Most other response features varied. Some units responded best to tone bursts, whereas others responded best to noise or band-limited noise (e.g., Fig. 2C). The low-frequency input could be either facilitatory or inhibitory. The tuning of these neurons to frequency ranges just below and above the first sonar harmonic (Fig. 1) suggests that they respond best to certain types of communication signals used by the mustached bat (Kanwal et al. 1994Functional organization
Study of the topographic distribution of auditory thalamic responses is based on 418 anatomically localized recording sites from 46 electrode penetrations. In the following text four aspects of organization are discussed: frequency organization in the MGB, distribution of combination-sensitive or other spectrally complex response properties in the MGB, distribution of sensitivity to delay among FM-FM responses, and responses of neurons in the thalamic reticular nucleus. Results are illustrated in Figs. 7-9 by penetrations throughout much the caudal to rostral extent of the MGB.
The MGB contains ventral, dorsal, and medial divisions (Fig.
5) as described previously
(Wenstrup 1995; Winer and Wenstrup 1994a
,b
). The ventral division is composed of lateral (Vl) and medial (Vm) parts. The dorsal division is large. Its major
subdivisions, the dorsal and rostral pole nuclei, dominate the rostral
half of the MGB. The medial division is small and few auditory
responses were recorded from it in this study. The description below
focuses on the distribution of responses in the ventral, dorsal, and
rostral pole nuclei of the MGB and in the thalamic reticular nucleus
(Table 2).
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FREQUENCY ORGANIZATION IN THE MGB.
Because many neurons in the MGB displayed two frequency tuning curves,
it is necessary to specify what is meant by frequency organization.
Considered here is the distribution of best frequencies among singly
tuned responses and the best high frequencies of combination-sensitive or multiply-tuned responses. For these complex responses, the best high-frequency response is used for two reasons: most recording sites displayed some responsiveness to the best high-frequency signal when it was presented separately, and
combination-sensitive MGB neurons receive their ascending input from
frequency representations of the central nucleus of the inferior
colliculus (ICC) corresponding to their best high-frequency response
(Wenstrup and Grose 1995). Consequently, this frequency
organization in MGB is comparable with the topographic pattern of
inputs from the tonotopically organized ICC.
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DISTRIBUTION OF COMPLEX SPECTRAL RESPONSE PROPERTIES IN THE MGB. A major finding was that combination-sensitive and other complex spectral response properties occurred in every subdivision of the MGB from which recordings were obtained (Table 2, Figs. 7-9). In most subdivisions, complex response properties predominated, ranging from 70 to 85% for Vm, the rostral pole and dorsal nuclei, and the thalamic reticular nucleus. Only in Vl were these responses in the minority. Different types of complex spectral responses characterized different subdivisions, the expected result of their frequency tuning. Thus FM-FM neurons were most common in the rostral part of the dorsal division because neurons responsive to frequency bands of the higher FM harmonics were most common there. H1-CF neurons were most common in Vm and dorsal and rostral pole nuclei of the middle one-third of the MGB. Nonsonar combination-sensitive neurons were most common in Vl.
Distribution of H1-CF responses. The data were examined for possible segregation of FM-CF and CF-CF neurons within different MGB nuclei, similar to what occurs in the mustached bat's auditory cortex (Fitzpatrick et al. 1998bAUDITORY RESPONSES IN THE THALAMIC RETICULAR NUCLEUS. In penetrations through the thalamus, acoustic responses were characterized at 28 recording sites histologically localized to the thalamic reticular nucleus. These showed a range of response properties similar to those recorded in the MGB. Latencies of 7-11 ms were recorded for four single units, a sample too small to judge the distribution. Eight responses were singly tuned to frequencies in the 23-45 kHz range. Ten showed FM-FM properties, ranging in best delay from 2-6 ms. Seven were H1-CF responses, and three had complex tuning to frequencies in the 15- to 23- and 33- to 45-kHz ranges. Thus the majority of acoustically responsive neurons in the thalamic reticular nucleus had complex frequency responses (71%, Table 2). The limited number of recordings precluded an indepth study of the distribution of these responses. Generally, recordings of higher frequency responses (>47 kHz) and sonar-related combination-sensitive responses (H1-CF and FM-FM) were placed more medially, as they were in the MGB (Figs. 7 and 8).
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DISCUSSION |
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Emphasizing responses to complex sounds, this study examined physiological properties and functional organization in the mustached bat's auditory thalamus. The study described types of combination-sensitive responses not previously reported in the MGB and showed that spectrally complex responses are common in and distributed widely throughout the MGB. The study also described distinct organizational features in different MGB divisions: the ventral division displays a modified tonotopic organization, while organization in the dorsal division appears to be related to the functional roles of the neurons in echolocation behavior.
Together with studies of the inferior colliculus and auditory cortex,
the present results help to identify the nature and site of
transformations in the representation of complex acoustic stimuli that
occur in the ascending auditory pathway of the mustached bat. Because
most complex response properties in the MGB and auditory cortex are
created in auditory centers below the MGB (Mittmann and Wenstrup
1995; Wenstrup and Grose 1995
) and show little
alteration between the ICC and MGB (Portfors and Wenstrup
1999b
), the major tecto-thalamic transformation appears to be a
reorganization of response properties, laying the groundwork for much
of the physiological organization within and across the different areas
of auditory cortex.
Physiological responses in the auditory thalamus
A major finding of this study is that combination sensitivity,
i.e., facilitated responses to (or inhibitory interactions between)
different spectral components of vocalizations, occurs throughout the
MGB. Combination-sensitive neurons are abundant in the rostral and
dorsal MGB, as reported previously (Olsen and Suga
1991a,b
), but also occur commonly in the ventral division, where more than half of the neurons are combination-sensitive. In
addition, more diverse types of combination-sensitive responses were
found, including responses to combinations of nonsonar frequency bands
that had not been reported previously. Finally, the thalamic reticular
nucleus showed a range of response properties similar to those recorded
in the MGB.
FM-FM NEURONS.
FM-FM neurons were recorded in both the dorsal division, as reported
previously (Olsen and Suga 1991b), and in the ventral division. Interactions between responses to FM1 and higher harmonic FM
signals were mostly facilitatory with few showing purely inhibitory responses to the FM1 signal. This predominance of facilitatory interactions appears similar to FM-FM regions of auditory cortex, where
inhibitory combination-sensitive interactions have not described, but
is distinguished from the inferior colliculus, where inhibitory interactions are more common (Portfors and Wenstrup
1999b
). Similar to a previous report (Olsen and Suga
1991b
), there was a broad distribution of best delays of 1-24
ms, with emphasis on delays of 1-10 ms. If best delays of these
neurons code for target distance, the population in the MGB represents
distances
4.1 m, with most neurons coding for distances of
1.7 m.
This range of best delays closely corresponds to the range of best
delays among FM-FM neurons in the inferior colliculus (Portfors
and Wenstrup 1999b
; Yan and Suga 1996
) and
auditory cortex (O'Neill and Suga 1982
; Suga and Horikawa 1986
) of the mustached bat. This similarity indicates that neural processing to create delay tuning is largely complete by
the level of the inferior colliculus.
H1-CF NEURONS.
Olsen and Suga (1991a) previously reported the presence
of facilitating CF-CF neurons in the dorsal division of the MGB. This study found that combination-sensitive responses to higher harmonic CF
signals (CF2, 60-63 kHz; CF3, 90-94 kHz) may be either facilitated or
inhibited by signals in the first sonar harmonic, and they are present
in both the ventral and dorsal divisions. Moreover, they showed a broad
range of tuning to the first harmonic frequencies, from 25 to 31 kHz,
indicating that both FM-CF and CF-CF neurons occur. Importantly, the
peak of the distribution was near 27.5 kHz, the frequency used in
earlier studies to distinguish between FM1-CF2 and CF1-CF2 responses in
auditory cortex (Fitzpatrick et al. 1993
). This suggests
that the distinction between these types, at least in the MGB, is not
clear cut, and it was for this reason that the present study used the
more general term H1-CF to designate all of these. The lack of clear
physiological distinctions suggests that the functional roles of many
H1-CF neurons in sonar are not well understood and that further study
is required.
NONSONAR COMBINATION-SENSITIVE RESPONSES.
MGB neurons tuned to combinations of frequency bands outside the sonar
range display facilitative or inhibitory interactions similar to sonar
combination-sensitive neurons. Most are tuned to both the 10- to 23- and 33- to 47-kHz frequency bands and are located in the ventral
division. They include distinct response types, one responding best to
combinations of tones, another responding better to noise bands than to
tones or their combinations. These nonsonar combination-sensitive
neurons are common in the inferior colliculus representation of 33-47
kHz, where they comprise 64% of a sample of 81 neurons (Leroy
and Wenstrup 1996; unpublished observations). These neurons may
analyze social vocalizations used by the mustached bat because many
signals include energy in both the 10- to 23- and 33- to 47-kHz bands
and can have either tonal or noise-like elements (Kanwal et al.
1994
). Such neurons have not been described previously in
either the MGB or auditory cortex, although neurons tuned to the 33- to
47-kHz band in AI are reported to display broad frequency tuning
(Fitzpatrick et al. 1998b
). These cortical neurons are
likely to show similar combination-sensitive responses as those in the
ICC or MGB. Thus basic features of complex responses to nonsonar
frequency bands, like those to sonar frequency bands, appear to
originate by the level of the ICC.
Physiological organization of the mustached bat's MGB
VENTRAL DIVISION.
The ventral division contains a tonotopic organization based on the
best frequencies of singly tuned neurons and the higher best
frequencies of combination-sensitive neurons (Fig. 10A).
Three features of this organization are noteworthy. First, few neurons are tuned to 24-31 kHz, the range of the first sonar harmonic. Second,
the 60-63 kHz (CF2 sonar component) representation is hypertrophied.
Third, the representations of 48-59, 72-89, and 96-119 kHz (higher
harmonic FM sonar components) are very small. The first two features
are similar to what has been observed in the ICC (O'Neill et
al. 1989; Zook et al. 1985
). However, the third
feature differs strikingly from what occurs in the ICC, where
frequencies in the ranges of the higher harmonic FM signals enjoy
substantial representations (O'Neill et al. 1989
).
DORSAL DIVISION: FREQUENCY ORGANIZATION. The frequency representation in the dorsal division is different from the ventral division. First, nearly all neurons (~90%) are tuned to frequencies within various harmonics of the sonar pulse, whereas ~66% of neurons in the ventral division are similarly tuned. Second, there is no tonotopic organization in the dorsal division. Third, there is a frequency organization apparently related to the functional role of frequency bands in biosonar. Thus neurons tuned to the frequency bands of the higher harmonic CF sonar components, at 60-63 or 90-94 kHz, are separated from neurons tuned to the bands of the higher harmonic FM components, at 48-59, 72-89, or 96-119 kHz, with little interdigitation between the CF- and FM-tuned populations.
For best frequencies tuned to the CF bands, the 60- to 63-kHz responses were consistently placed more dorsally and laterally than the 90- to 94-kHz responses. For FM-tuned best frequencies, the topographic distribution is quite complex. Responses to each of the FM frequency bands appeared to be distributed in at least two areas of the dorsal division, as described in RESULTS (Fig. 10A). The dorsal division of the MGB receives strong input from the ICC (Frisina et al. 1989DORSAL DIVISION: ORGANIZATION OF COMBINATION-SENSITIVE RESPONSES.
Because some areas of auditory cortex are reported to be organized by
specific response properties of combination-sensitive neurons, this
section considers whether similar arrangements occur in the dorsal
division. Among neurons sensitive to CF components in sonar signals, no
further organization of combination-sensitive responses was found. In
the dorsal and rostral pole nuclei, as in the ventral division, CF1-CF
responses were intermixed with FM1-CF responses. Thus there is no
correspondence in the MGB to the reported segregation of FM1-CF
responses (in AI and a ventral cortical area) and CF1-CF responses (in
the CF-CF area and another ventral cortical area) (Fitzpatrick
et al. 1993, 1998b
; Suga et al. 1983
).
Furthermore there was no indication that CF-CF neurons in MGB are
organized along the axis of relative (Doppler) frequency shifts, as has
been described in the CF-CF area of auditory cortex (Suga et al.
1983
). Such an organization in the MGB may well be too
fine-grained to be detected by the methods of this study, yet the lack
of segregation of CF1-CF neurons from FM1-CF neurons suggests that a
comparable thalamic organization is unlikely. To create the topographic
features described in auditory cortex, the output of the MGB would
require reorganization.
Auditory thalamic organization: species comparisons
A major feature of MGB organization among mammals concerns
differences between the ventral division and the dorsal and medial divisions. In the ventral division, the laminar arrangement of principal cell dendrites (Morest 1965; Winer
1992
) is thought to provide a substrate for the tonotopic
organization that has been observed in several species (Aitkin
and Webster 1972
; Clarey et al. 1992
).
Physiologically, ventral division neurons typically display sharp
frequency tuning, relatively short latencies, good temporal precision,
and consistent responses to repetitive sounds. In contrast, the dorsal
and medial divisions do not typically display similar clear tonotopic
organizations, and their responses are on average more broadly tuned in
frequency, longer in latency, less temporally precise, and less
consistent (Aitkin 1973
; Aitkin and Webster
1972
; Calford 1983
; Clarey et al.
1992
; Lennartz and Weinberger 1992
).
In the mustached bat, the clearest similarity to this general mammalian
plan is the different functional organizations of the ventral and
dorsal divisions. The present study shows that the ventral division is
tonotopically organized, whereas the dorsal division contains no
similar physiological organization. However, even these similarities to
the general mammalian plan have a strong species-specific character.
The tonotopic organization in the ventral division, with its lack of
neurons tuned to sonar FM frequency bands, is changed markedly from the
ICC (O'Neill et al. 1989; Zook et al.
1985
). Moreover, the nontonotopic frequency organization in the
dorsal division segregates neurons on the basis of the sonar components
they analyze and appears to organize a population of these (FM-FM
neurons) according to a response property related to the analysis of
sonar targets (delay tuning).
A distinctive feature of the mustached bat's MGB is the prevalence of
complex spectral responses in both the ventral and dorsal divisions (58 and 79%, respectively). Most of these are facilitated, combination-sensitive responses to the frequency range of biosonar signals. Although such responses are more common in the dorsal division, both divisions have a majority of complex spectral responses. In other mammals, the majority of ventral division neurons display a
single, relatively narrow, excitatory tuning curve, whereas multipeaked
tuning curves are more common in the dorsal and medial divisions
(Aitkin 1973; Aitkin and Webster 1972
;
Calford 1983
; Calford and Webster
1981
; Imig and Morel 1985
;
Lennartz and Weinberger 1992
). Some of these may be
combination-sensitive. In the squirrel monkey MGB, neurons responsive
to combinations of different temporal and spectral elements in social
vocalizations have been recorded in preliminary studies (Olsen
1994
). However, even in the dorsal division of other mammals,
stimulus specificity for complex sounds and overall numbers of neurons
with multipeaked tuning curves do not approach the proportions found
here in the mustached bat dorsal division.
This difference may result from the mustached bat's reliance on
multiharmonic vocalizations for both orientation and communication, but
it may result in part from the use of barbiturate anesthetics in many
studies on other species. In the MGB of cats and monkeys, the
complexity of both single-unit frequency tuning and tonotopic organization is greater when obtained from unanesthetized or lightly anesthetized animals (Allon et al. 1981; Morel et
al. 1987
). For example, in lightly anesthetized cats, nearly
20% of ventral division neurons displayed multipeaked tuning curves
and ~40% had "broad" frequency tuning. For medial division
neurons in the same study, nearly 80% had either broad or multipeaked
tuning curves.
The species-specific patterns in the mustached bat appear closely
related to the physiology and projection patterns of neurons in the
inferior colliculus. The clear majority of neurons in the mustached
bat's ICC, whether in the regions analyzing sonar calls (Mittmann and Wenstrup 1995; Portfors and
Wenstrup 1999
) or in nonsonar regions (Leroy and
Wenstrup 1996
), contain combination-sensitive or other
spectrally complex (e.g., multipeaked tuning curves) responses.
Furthermore, these ICC neurons provide the major projection to both the
ventral and dorsal divisions, and their topographic patterns of input
determine the frequency organization of both the ventral and dorsal
divisions (Wenstrup and Grose 1995
; Wenstrup et
al. 1994
). In contrast, the dorsal division in other species typically receives stronger input from other parts of the inferior colliculus, such as the dorsal cortex and external nucleus
(Oliver and Huerta 1992
; Winer 1992
). It
is unclear whether the physiological properties of these regions confer
the broader frequency tuning and less precise temporal response
features onto dorsal and medial division neurons or whether these are
created by integration of inputs in the MGB.
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ACKNOWLEDGMENTS |
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I thank Z. M. Fuzessery and C. V. Portfors for helpful comments on the manuscript, C. D. Grose for technical assistance, F.-M. Chen for the software, and the Natural Resources Conservation Authority of Jamaica for permission to collect the bats.
This work was supported by Grant 5 R01 DC-00937 from the National Institute on Deafness and Other Communication Disorders and by a Research Challenge Grant from the Ohio Board of Regents.
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FOOTNOTES |
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Address for reprint requests: Dept. of Neurobiology, Northeastern Ohio Universities College of Medicine, 4209 State Route 44, P.O. Box 95, Rootstown, OH 44272-0095.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement " in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 30 November 1998; accepted in final form 7 July 1999.
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REFERENCES |
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