Department of Psychology, University of Colorado at Boulder, Boulder, Colorado 80309, USA
Address correspondence to Dr Daniel S. Barth, Department of Psychology, University of Colorado, Campus Box 345, Boulder, CO 80309-0345, USA. Email: dbarth{at}psych.colorado.edu.
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Abstract |
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Key Words: AII auditory barrel polysensory SII
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Introduction |
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The functions of both SII and AII are poorly understood. Yet there is evidence that one of the roles may be in multisensory integration. Based on microelectrode recordings in the rat, Wallace et al. (2004) recently proposed a revised view of sensory cortical parcellation in which the cortical regions bordering and interposed between unisensory regions are predominately multisensory. Since the interposed cortex largely overlaps presumed SII and AII, it is not surprising that many studies of secondary sensory cortex have reported at least partially overlapping multisensory responsive zones (Woolsey and Wang, 1945
; Woolsey and Fairman, 1946
; Lende and Woolsey, 1956
; Pinto-Hamuy et al., 1956
; Woolsey, 1958
; Berman, 1961a
,b
; Carreras and Andersson, 1963
; Lende, 1963
; T.A.Woolsey, 1967
; Campos and Welker, 1976
; Pubols, 1977
; Burton et al., 1982
; Clemo and Stein, 1983
; Carvell and Simons, 1986
). This raises the question of whether multisensory integration should be considered to be a function of secondary sensory cortex, or if multisensory cortex should be regarded as functionally and anatomically distinct, with secondary cortex performing more unisensory processing tasks.
In the present study, we used high-resolution epipial field potential mapping of somatosensory and auditory evoked potentials (SEP and AEP, respectively) in rodent lateral parietotemporal cortex to determine areas of unisensory and multisensory responsiveness. We applied multivariate statistical analysis to determine the significance and reliability of somatotopic representations in these areas, and then used the results to guide placement of a laminar microelectrode array to record localized field potentials and multiunit activity (MUA) from putative unisensory and multisensory zones.
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Materials and Methods |
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All procedures were performed in accordance with University of Colorado Institutional Animal Care and Use Committee guidelines for the humane use of laboratory animals in biological research. Adult male SpragueDawley rats (300400 g) were anesthetized to surgical levels using intramuscular injections of ketamine (71 mg/kg body wt), xylazine (14 mg/kg) and acepromazine (2.4 mg/kg), placed on a regulated heating pad and maintained with subsequent injections throughout the experiment so that the eye blink reflex could be barely elicited. A unilateral craniectomy was performed over the left hemisphere extending from bregma to lambda and from the midsagittal sinus laterally beyond the temporal bone to within 0.5 mm of the rhinal sulcus, exposing a wide region of parietotemporal cortex where the dura was reflected. Animals were sacrificed by anesthesia overdose without regaining consciousness at the conclusion of the experiment.
Stimulation
Auditory click stimuli were delivered with a high frequency piezo-electric speaker aligned with, and 10 cm from, the contralateral ear. The ipsilateral ear was blocked with soft wax. Clicks were computer-controlled monophasic square-wave pulses (0.3 ms;
50 db SPL at 10 cm). Silent stimulation of the large vibrissae on the contralateral mystacial pad was achieved using a laboratory built solenoid with attached 3 cm hypodermic tubing. In most rats, stimulation displaced the tied vibrissae as a group vertically by
0.5 mm. In several rats, similar stimulation was applied to four subgroups of three tied vibrissae each that were situated in the extreme rostral, caudal, dorsal and ventral regions of the contralateral vibrissa array. During vibrissa stimulation, bilateral wax earplugs were also fitted to assure no incidental auditory stimulation. Silence was verified by observing activity in auditory cortex when the solenoid was close to, but not touching, the vibrissae. Silent electrical stimulation of discrete body regions (forepaw, forelimb, midtrunk, hindpaw and hindlimb) was achieved with a bipolar stainless steel electrode (0.5 mm separation; 1 mm exposed tip) attached to a constant current source, delivering current pulses (1 ms) of minimum current (0.20.5 mA) required to produce a reliable evoked response with no noticeable muscle contractions when applied to the shaved skin pretreated with conductive jelly. Electrical stimulation sites were on the back of the forepaw and hindpaw, on the proximal part of the forelimb and hindlimb, and on the lateral trunk midway between the forelimb and hindlimb. While stimulation produced no noticeable muscle contractions, activation of other afferents besides cutaneous could not be ruled out.
Data Collection and Analysis
Epipial maps of AEP and SEP were recorded using a flat multi-electrode array consisting of 64 silver wires in an 8 x 8 grid (tip diameter: 100 µm; impedance:
1 k
at 1 kHz; inter-electrode spacing: 500 µm) covering a 3.5 x 3.5 mm area. Surface AEP were used to consistently align the array across animals. Laminar recordings were performed with a 16 contact (10 µm diameter, impedance:
1 m
at 1 kHz; 100 µm spacing) linear array (University of Michigan Center for Neural Communication Technology), inserted perpendicular to the cortical surface to a depth where the uppermost electrode was barely visible at the cortical surface. Visibility of the uppermost electrode was checked throughout the experiment. Recordings of epipial and laminar potentials were referred to a silver ball electrode secured over the contralateral frontal bone, and were simultaneously amplified (x10 000), analog filtered (band-pass cut-off = 6 dB at 0.001 to 3000 Hz, roll-off = 5 dB/octave) and digitized at 10 kHz. Trials of separately evoked epipial AEP or SEP were averaged over 100 presentations. During laminar recording, 100 single trial records of AEP and SEP were stored on disk for subsequent analysis. This consisted of simple averaging of field potentials. MUA was also computed by digitally high-pass filtering (1000 Hz) and rectifying each trial and then averaging across trials for a given stimulus condition and recording location. Given the 10 µm diameter and 1 m
impedance of the laminar electrode contacts, MUA was assumed to reflect activity of larger clusters of units than would be expected from higher impedance microelectrode recordings.
The location and spatial distribution of epipial evoked responses was determined from interpolated (bicubic spline) topographic maps depicting the root mean squared (RMS) power of the response at each electrode, computed within the first 1325 ms post-stimulus so that only the initial positive deflection (P1) was included. This constraint was introduced because the earliest temporal component is the most spatially constrained and best reflects initial cortical activation, before substantial intracortical propagation that produces the later temporal components of the slow wave. Putative multisensory regions were identified by similarly mapping a function computed from the relative AEP and SEP power at each electrode location, reflecting areas where auditory and somatosensory responses overlapped and were of large amplitude, using the following equation:
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Laminar recordings were performed at field potential maxima for presumed unisensory and multisensory cortex for a given body part, as determined from epipial maps for each animal. Amplitudes of the averaged laminar AEP and SEP and corresponding MUA were compared by summing the RMS power throughout the 100 ms sampling epoch across all 16 electrode locations (RMSAEP and
RMSSEP, respectively). The relative amplitudes of the AEP and SEP at a given recording site were determined as the ratio
RMSAEP/
RMSSEP x 100, reported as mean (± SE) percent and compared between regions using unpaired t-tests with significance set to P
0.05. The expectation was that both field potentials and MUA would show a significantly reduced auditory/somatosensory ratio in more unisensory secondary somatosensory cortex compared with multisensory regions where the responses would be closer to equal power.
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Results |
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All animals receiving stimulation of the combined vibrissae (Fig. 1D; Vib-all) also received stimulation of the forepaw, forelimb, midtrunk, hindpaw and hindlimb (Fig. 1E; Fp, Fl, Mt, Hp, and Hl, respectively) and were studied with both epipial and laminar recordings. Spinal responses in SII were lateral to the vibrissa response, with Fp and Fl rostral to Mt, Hp and Hl. Each SEP map reflected a single representation for each body part that extended caudally to partially overlap the AEP. This caudal extension was particularly evident for Fp and Fl (Fig. 1E; arrows) where there was the greatest separation between unisensory and multisensory regions. Similar to Vib-all, regions where these responses overlapped the AEP (multisensory cortex) were shifted caudally, with Fp and FL just lateral to Vib and Mt, Hp and Hl most lateral.
To estimate the locus and extent of AI, SII and intervening multisensory cortex for the body parts stimulated here, composite maps were computed by averaged responses across animals and across all body parts stimulated (Fig. 2A; the approximate borders of each area indicated by dashed white outlines drawn along the 25% isocontour lines). Superimposed responses for each body part in SII, averaged across animals (Fig. 2A; SEP; dots), suggested a somatotopic map. The most rostral response was Fp, with the representation of Fl positioned at a distance of.15 ± 0.06 mm in the caudal and lateral direction, but this was not sufficiently separated to reach significance (P > 0.05, F = 3.2, df = 5). Responses to Hp, Hl and Mt were caudal to Fl (0.69 ± 0.12 mm, P < 0.001; 0.70 ± 0.11 mm, P < 0.001; 0.77 ± 0.10 mm, P < 0.001, respectively). Here, a significant medial to lateral organization was observed, with Hl located lateral to Hp by 0.22 ± 0.05 mm (P < 0.04) and Mt located lateral to Hl by 0.18 ± 0.07 mm (P < 0.04). The vibrissa representation was approximately aligned with Hp on the rostro-caudal axis, but was shifted medially by 1.64 ± 0.15 mm (P < 0.001). The somatotopic organization of spinal input to SII therefore appeared inverted, with the forelimbs oriented rostrally, the paws pointing medially.
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Figure 2B displays an example of laminar field potential and MUA profiles in the unisensory vibrissa representation of SII and the more caudal region of AEPSEP overlap. Here, and in field potential recordings of other body representations, the surface recorded P1 and subsequent negative wave (N1) reversed polarity in the depth (Fig. 2C), indicating a cortical dipolar generator. In this example, at the location where the AEP and vibrissa evoked SEP overlapped at the surface, AEP power throughout the depth was 54% that of the SEP (Fig. 2C; right traces). In recordings performed
0.5 mm rostral to this site in SII, the power of the laminar SEP increased while the relative power of the AEP dropped to 2% of the SEP (Fig. 2C; left traces). The relative power of AEP and SEP field potentials in SII and multisensory cortex were reflected in corresponding laminar MUA activity. At the multisensory site, total MUA power evoked by auditory stimulation was
66% of that evoked by vibrissa stimulation (Fig. 2D: right traces). By contrast, in the vibrissa representation of SII, somatosensory MUA power nearly doubled while the relative auditory MUA power dropped to 5% of that evoked by somatosensory stimulation (Fig. 2D; left traces).
Relative powers of auditory and somatosensory responses differed in a similar way during laminar recordings in representations of the other body parts (Fig. 2E,F). In all cases, the ratio of auditory to somatosensory field potentials and MUA were significantly lower in SII compared with multisensory recording sites. The ratios of AEP to SEP in multisensory cortex were 89 ± 9, 85 ± 10, 82 ± 12, 140 ± 11, 120 ± 19 and 127 ± 13%, for Vib, Fl, Fp, Mt, Hl and Hp, respectively (Fig. 2E; red bars). These ratios dropped to 29 ± 4, 49 ± 6, 45 ± 4, 98 ± 9, 71 ± 11 and 70 ± 7%, for representations of the same body parts in SII (Fig. 2E; blue bars). Laminar MUA followed the field potential responses with ratios of auditory to somatosensory equaling 73 ± 9, 73 ± 13, 66 ± 8, 100 ± 17, 92 ± 26 and 93 ± 22%, for Vib, Fl, Fp, Mt, Hl and Hp representations in multisensory cortex (Fig. 2F; red bars) and 29 ± 4, 44 ± 8, 42 ± 6, 56 ± 9, 40 ± 6 and 43 ± 8%, for corresponding representations in SII (Fig. 2F; blue bars).
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Discussion |
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Overlap between secondary somatosensory and auditory cortex has been variously described (Woolsey and Wang, 1945; Woolsey and Fairman, 1946
; Lende and Woolsey, 1956
; Pinto-Hamuy et al., 1956
; Woolsey, 1958
; Berman, 1961a
,b
; Carreras and Andersson, 1963
; Lende, 1963
; T.A.Woolsey, 1967
; Campos and Welker, 1976
; Pubols, 1977
; Clemo and Stein, 1983
; Carvell and Simons, 1986
). In light of the rostral orientation of SII, it is perhaps not surprising that the region of somatosensoryauditory overlap typically involves the trunk and hindquarters, which are positioned closest to auditory cortex. However, the present data suggest that multisensory cortex forms a complete and separate somatotopic map, including even the most rostral anatomical representations such as the forelimbs and rostral vibrissa group. This conclusion is further supported by laminar field potential and MUA recordings indicating a multisensory responsiveness within this region that may be distinguished from more unisensory responses even for the trunk and hindquarters where the epipial SEP and AEP almost completely overlap. In this light, the area of multisensory cortex in the rat may be analogous to multisensory cortex (SIV) in the cat (Dehner et al., 2004
) and the ventral somatic area (VS) of the monkey (Coq et al., 2004
), which are distinguished by their complete somatotopic representations, proximity to auditory belt cortex and unique auditory/somatosensory responsiveness.
The position of multisensory cortex at the rostral border of AI overlaps auditory belt cortex. Multisensory cortex therefore probably receives auditory input from the acoustic thalamus (Ryugo and Killackey, 1974; Winer and Larue, 1987
; Arnault and Roger, 1990
; Brett et al., 1994
) as well as input from somatosensory thalamus (Brett-Green et al., 2003
). Injections of anatomical tracer into a similar locus in the grey squirrel (area PV; Krubitzer et al., 1986
) labeled regions of somatosensory thalamus (the ventral posterior complex and ventral posterior inferior nucleus) as well as auditory thalamus (medial geniculate interior nucleus; (Krubitzer and Kaas, 1987
). Studies in the cat have suggested that SII should be considered structurally and functionally distinct from SIV, based on differential thalamocortical connectivity. SII receives projections mainly from the posteromedial ventral nuclei (VPL, VPM) of somatosensory thalamus, whereas multisensory SIV receives projections from the VPL, VPM and posterior nuclei (PO) of somatosensory thalamus, as well as the magnocellular medial geniculate (MGm) and suprageniculate (SG) nuclei of auditory thalamus (Burton et al., 1982
; Roda and Reinoso-Suárez, 1983
; Niimi et al., 1987
). The present results provide functional evidence supporting the segregation of SII and multisensory cortex in the rat. They also demonstrate the effectiveness of high-resolution epipial evoked potential mapping for distinguishing SII from multisensory cortex and for precisely guiding laminar electrode recordings in these separate regions. These results provide a foundation for using the same methods to guide histological tracer injections and examine differences in intracortical and thalamocortical connectivity of these areas. Area 36 of secondary auditory cortex appears to be unisensory and receives projections from the dorsal division of the medial geniculate nucleus (Patterson, 1977
). It will be informative to see if unisensory SII may be similarly distinguished from multisensory cortex based on its preferred connections with unisensory somatosensory thalamus.
Our data fit a plan in which multisensory areas are interposed between unisensory cortices (Wallace et al., 2004), including secondary cortex. Multisensory cortex may be functionally and anatomically distinct, with secondary cortex performing more unisensory processing tasks. Distinct unisensory and multisensory pathways are not unique to the cerebral cortex and have also been identified in subcortical structures such as the thalamus (Winer and Morest, 1983
; Steriade et al., 1997
). Perhaps one of the most thoroughly studied centers for multisensory integration is the superior colliculus (Anasasio and Patton, 2004
; Stein et al., 2004
). Similar to the cortex, trigeminal input, particularly from the vibrissae, is disproportionately represented in deep layers of the rat superior colliculus, reflecting its importance in combination with auditory and visual senses for environmental exploration and orienting to novel stimuli. Yet even here, there is evidence that processing of at least nociceptive information from the face has evolved as an essentially unisensory task concerned predominantly with nocifensive reactions to proximal harmful stimuli (McHaffie et al., 1989
). Our data suggest that analogous evolutionary influences may be at work in the segregation of multisensory and unisensory cortex in the rat. It has been proposed that evolutionary advances of cortical structures may be directed toward less multisensory integration and more unisensory segregation (Diamond and Hall, 1969
), a process that could be justified by the challenges inherent to accurately identifying objects in a particular sensory modality compared with co-registering these objects in multisensory space. In this light, the rat may reflect a transitional phase, where the cortical processing of the face and forelimbs, most important for exploration of the environment, has become distinctly segregated into unisensory and multisensory regions of parietotemporal cortex with substantially less segregation of the hindquarters.
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Acknowledgments |
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