W.M. Keck Center for Integrative Neuroscience, University of California San Francisco, San Francisco, CA 94143-0732, USA
Address correspondence to Dr Jennifer F. Linden, Keck Center for Integrative Neuroscience, University of California San Francisco, Room HSE804, 513 Parnassus Avenue, San Francisco, CA 941430732, USA. Email: linden{at}phy.ucsf.edu.
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
![]() |
Cortical Circuitry |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Other features of auditory cortical circuitry also seem to differ substantially from the anatomy of visual and somatosensory cortices. For example, spiny stellate cells, which dominate layer IV of the visual and somatosensory cortices in most species (Jones, 1975; Lund et al., 1979
; Simons and Woolsey, 1984
) are largely absent from the middle layers of cat primary auditory cortex (Smith and Populin, 2001
). In their place, small pyramidal cells in lower layer III and layer IV appear to be the chief thalamorecipient neuron in auditory cortex (Smith and Populin, 2001
). The broader than expected laminar distribution of lemniscal thalamic input to auditory cortex supports this hypothesis. In contrast to visual cortex and barrel cortex, in which the primary thalamic input terminates mainly in layer IV (LeVay and Gilbert, 1976
; Landry and Deschênes, 1981
), the lemniscal thalamic input to auditory cortex extends well into layer III (Winer, 1992
; Huang and Winer, 2000
). Another unusual feature of the auditory thalamocortical projection arises outside the lemniscal pathway: giant axons ascending from a non-lemniscal part of the auditory thalamus to layer I of auditory cortex appear to be unique to the auditory system, and may carry some of the earliest thalamic signals into auditory cortex (Huang and Winer, 2000
).
Like the anatomy, the intrinsic properties and synaptic physiology of auditory cortex resemble those of other primary sensory cortices, with some intriguing differences. In vitro studies of auditory cortex (Metherate and Aramakis, 1999; Hefti and Smith, 2000
, 2002
) have identified classes of regular-spiking, fast-spiking and intrinsic-bursting cells seen in other cortical areas (McCormick et al., 1985
; Connors and Gutnick, 1990
). However, such studies have also found that inhibitory response kinetics are much faster in auditory cortex (Hefti and Smith, 2002
), and that auditory cortex may have a unique class of neurons that spikes very briefly upon depolarization and then shows strong outward rectification suppressing further spiking (Metherate and Aramakis, 1999
). Furthermore, a recent investigation of synaptic transmission found that layer II/III pyramidal neurons in auditory cortex were connected by synapses displaying low release probability and minimal short-term depression, as well as by high-probability depressing synapses (Atzori et al., 2001
); only the latter type of synaptic transmission was observed in barrel cortex.
Since in vitro slice experiments are typically conducted in immature animals, these apparent physiological differences between auditory cortex and other sensory cortices might be an artifact of different maturational rates for each modality (Stern et al., 2001; Zhang et al., 2001
; Desai et al., 2002
). However, it is also possible that the unusual electrophysiological characteristics of auditory cortex neurons reflect unique features of auditory cortical processing. For example, ultra-rapid inhibition and a wide diversity of synaptic transmission characteristics might contribute to specialization of auditory cortex for fast temporal information processing (Buonomano, 2000
). The recent development of an auditory thalamocortical slice preparation (Cruikshank et al., 2002
) promises new insights into the nature of auditory cortical physiology, and further modality comparisons through parallel experiments on auditory and somatosensory thalamocortical slices (Agmon and Connors, 1991
).
![]() |
Thalamocortical and Intracortical Transformations |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The various auditory thalamocortical transformations demonstrated by Miller and colleagues (Miller et al., 2001) involved primarily the excitatory portions of thalamic and cortical receptive fields. Inhibitory subregions of paired thalamic and cortical receptive fields appear to be less closely related, and many receptive-field properties that depend on inhibitory subfield arrangements (e.g. temporal and spectral modulation preferences) are poorly conserved in auditory thalamocortical transformations (Miller et al., 2001
). Perhaps the inhibitory subregions of cortical receptive fields (and associated neuronal response properties) are generated intracortically, through disynaptic interactions involving thalamic input onto inhibitory interneurons that synapse onto pyramidal cells within the same cortical layer. Such intracortical inhibition may shape cortical responses in thalamorecipient layers of auditory cortex, much as it is thought to do so in layer IV of visual cortex (Somers et al., 1995
; Hirsch et al., 1998
; Troyer et al., 1998
) and barrel cortex (Brumberg et al., 1996
; Pinto et al., 2000
; Swadlow and Gusev, 2000
).
How are receptive fields in thalamorecipient layers of auditory cortex transformed by further intracortical columnar processing? As mentioned in the introduction, previous studies of laminar differences and columnar processing in auditory cortex have failed to produce a consensus on how auditory receptive fields might differ across cortical layers. Studies of cat auditory cortex have reported layer-dependent variations in minimum response latency, with the shortest latencies in the thalamorecipient middle layers (Phillips and Irvine, 1981; Mendelson et al., 1997
), but investigations of rodent auditory cortex find the shortest response latencies in deeper layers [Mongolian gerbil (Sugimoto et al., 1997
); mouse (Shen et al., 1999
)]. Laminar differences in frequency tuning bandwidths, intensity thresholds and other response properties have been observed in some studies of cat, bat and rodent auditory cortex (Oonishi and Katsuki, 1965
; Eggermont, 1996
; Dear et al., 1993
; Sugimoto et al., 1997
), but not in other studies of the same species (Abeles and Goldstein, 1970
; Phillips and Irvine, 1981
; Jen et al., 1989
; Clarey et al., 1994
; Foeller et al., 2001
). Meanwhile, investigations in awake monkey cortex have recently reported systematic layer-dependent variations in binaural interactions (Reser et al., 2000
), and have suggested that such laminar differences might have been masked in earlier experiments by the confounding effects of anesthesia.
Even if effects of anesthesia explain some of the discrepancies in the literature, the lack of a consensus regarding laminar differences in auditory cortex contrasts markedly with the situation for visual and barrel cortex. Although controversies about the nature of intracolumnar transformations in those systems are far from resolved, the existence of laminar differences in stimulus sensitivities is beyond dispute. Indeed, laminar differences in visual cortex and barrel cortex (of both anesthetized and awake animals) have inspired many hypotheses about columnar function in those modalities. For example, the layer-dependent distribution of simple and complex cells in cat visual cortex, with simple cells predominating in the input layers and complex or hypercomplex cells more prevalent in superficial or deep layers, prompted Hubel and Wiesel to propose that complex cell receptive fields emerge through convergence of simple cell inputs within a column (Hubel and Wiesel, 1962). Their hypothesis has received experimental support from recent studies (Alonso and Martinez, 1998
; Martinez and Alonso, 2001
), although the influences of nonlinear dendritic interactions and recurrent connections on complex receptive-field structure are still much debated (Mel et al., 1998
; Chance et al., 1999
). In barrel cortex, the anatomical and physiological differences between layer IV and superficial or deep layers have also inspired hypotheses regarding columnar computation in this system. For example, the superficial and deep layers, which contain neurons with complex multi-whisker receptive fields, may construct dynamic representations of behaviorally relevant stimuli from the more precise single-whisker representations that predominate in layer IV (Simons, 1978
; Brumberg et al., 1999
). A complementary hypothesis is that the different layers of barrel cortex support parallel processing of spatial and temporal tactile information (Ahissar et al., 2000
, 2001
),
Is auditory cortex inherently more homogeneous across cortical layers than these other sensory cortices? As discussed previously, auditory cortical circuitry does have some unique features, but the fundamental similarities with other sensory cortices seem far more striking than these differences. Studies in which auditory thalamocortical pathways are modified experimentally (rewired) to receive visual signals further suggest that auditory cortex is capable of supporting the thalamocortical and intracolumnar transformations that produce laminar differences in other modalities. When retinal inputs are routed into the auditory thalamus after deafferentation of the normal brainstem inputs to the structure (Sur et al., 1988; Angelucci et al., 1998
), auditory cortical cells develop visual response properties such as direction selectivity, orientation tuning and simple/complex receptive-field structure (Roe et al., 1992
). Retinotopic maps of orientation tuning, complete with lateral connectivity between orientation domains, emerge in superficial layers of the rewired auditory cortex (Roe et al., 1990
; Sharma et al., 2000
). While laminar differences in rewired AI have not yet been systematically explored, the observed physiological parallels with VI suggest similar underlying intracolumnar transformations, and provide compelling evidence for common principles of columnar organization linking sensory cortical structures in different modalities.
If laminar organization in auditory cortex is not inherently more homogeneous than that in other sensory cortices, then what is the explanation for the lack of consensus regarding laminar differences? It is possible that auditory stimuli, recording methods or experimental conditions in previous studies have not usually been sufficient or consistent enough to reveal compelling laminar differences, and that further progress awaits the use of new and more sophisticated stimulus sets, novel experimental techniques for recording simultaneously within a column, or simply more data from more species under awake as as well as anesthetized conditions. Another possibility, however, is that cortical processing of auditory information drives functional organization in cortex that obscures laminar differences. Most previous studies of laminar differences in auditory cortex have examined sequential recordings from single-electrode penetrations, but then pooled data taken from penetrations at different sites across cortex in attempting to identify systematic laminar differences. Perhaps the substantial variability in response properties within thalamorecipient layers of auditory cortex (Fig. 3) greatly exceeds the variability in response properties across cortical layers. Definition of systematic laminar differences in auditory cortex may be possible only within small subregions of the overlapping stimulus feature maps (Fig. 1
) in which variability within each cortical layer is minimized.
|
![]() |
Future Directions |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
To the extent that such direct receptor-level analogies to the visual and somatosensory systems are appropriate, then one would expect several stimulus features to vary in their representation across layers in auditory cortex. Visual and somatosensory receptive-field sizes tend to be smallest in layer IV (Gilbert, 1977; Simons, 1978
; Sur et al., 1985
; Métin et al., 1988
), suggesting that the spectral integration bandwidths of auditory cortical neurons should be narrowest in the middle layers. Neurons sensitive to high speeds of visual motion are found most often in supra- and infragranular layers of visual cortex (Gilbert, 1977
; Mangini and Pearlman, 1980
), so perhaps a similar laminar distribution would be expected for auditory cortex neurons sensitive to fast frequency sweeps. Laminar differences in temporal frequency tuning in barrel cortex (Ahissar et al., 2001
) imply that receptive fields in different layers of auditory cortex could have distinct preferences for rates of amplitude modulation. Variations with cortical depth in the strength of orientation tuning in visual cortex (Mangini and Pearlman, 1980
; Martinez et al., 2002
; Ringach et al., 2002
) and somatosensory cortex (Simons, 1978
; Chapin, 1986
; DiCarlo and Johnson, 2002
) might have an auditory parallel in the laminar distribution of auditory receptive fields with pronounced and/or asymmetric inhibitory sideband structure. Finally, the layer-dependent distribution of simple and complex cells in visual cortex (Hubel and Wiesel, 1962
; Gilbert, 1977
) suggests that a similar distribution of linear and nonlinear response types might be found in auditory cortex. Simple and complex visual neurons are distinguished by their relative sensitivity to the spatial phase of an oriented stimulus; auditory cortex analogs might show varying sensitivity to the phase of spectral ripple, or perhaps to the phase of frequency and amplitude modulations.
Ultimately, however, these receptor-level analogies may prove less useful as a guide to understanding columnar transformations in auditory cortex than a more functional, modality-specific approach inspired by another observation from studies of visual and somatosensory cortices: the apparent relevance of columnar structure to experience-dependent sensory processing. Experience-dependent plasticity in receptive-field structure follows layer-dependent time courses in both visual cortex (Daw et al., 1992; Trachtenberg et al., 2000
; Desai et al., 2002
) and barrel cortex (Diamond et al., 1994
; Stern et al., 2001
). These findings suggest that experience may shape and underlie the function of cortical columns in any cortical structure. Indeed, experiments in congenitally deafened cats have already demonstrated that auditory experience plays a crucial role in development of normal patterns of laminar activation in auditory cortex (Kral et al., 2000
). Other studies of experience-dependent plasticity in auditory cortex (Recanzone et al., 1993
; Weinberger, 1998
; Kilgard et al., 2001
; Zhang et al., 2001
) have documented profound changes in frequency tuning, repetitionrate tuning and other auditory receptive-field properties after behavioral training or other manipulations of auditory experience, but such studies have largely omitted any systematic exploration of the effects on a laminar basis. Critical insights into the function of cortical columns in auditory cortex may come, not from strict receptor-level analogies to the roles of cortical columns in visual and somatosensory processing, but from a natural extension of the rich history of work on cortical plasticity to pinpoint the roles of different cortical layers in auditory learning.
![]() |
Footnotes |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Agmon A, Connors BW (1991) Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41:365379.[CrossRef][ISI][Medline]
Ahissar E, Sosnik R, Haidarliu S. (2000) Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature 406:302306.[CrossRef][ISI][Medline]
Ahissar E, Sosnik R, Bagdasarian K, Haidarliu S (2001) Temporal frequency of whisker movement. II. Laminar organization of cortical representations. J Neurophysiol 86:354367.
Alonso JM, Martinez LM (1998) Functional connectivity between simple cells and complex cells in cat striate cortex. Nat Neurosci 1:395403.[CrossRef][ISI][Medline]
Alonso JM, Usrey WM, Reid RC (2001) Rules of connectivity between geniculate cells and simple cells in cat primary visual cortex. J Neurosci 21:40024015.
Angelucci A, Clasca F, Sur M (1998) Brainstem inputs to the ferret medial geniculate nucleus and the effect of early deafferentation on novel retinal projections to the auditory thalamus. J Comp Neurol 400:417439.[CrossRef][ISI][Medline]
Atzori M, Le S, Evans DI, Kanold PO, Phillips-Tansey E, McIntyre O, McBain CJ (2001) Differential synaptic processing separates stationary from transient inputs to the auditory cortex. Nat Neurosci 4:12301237.[CrossRef][ISI][Medline]
Brugge JF, Merzenich MM (1973) Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. J Neurophysiol 36:11381158.
Brumberg JC, Pinto DJ, Simons DJ (1996) Spatial gradients and inhibitory summation in the rat whisker barrel system. J Neurophysiol 76:130140.
Brumberg JC, Pinto DJ, Simons DJ (1999) Cortical columnar processing in the rat whisker-to-barrel system. J Neurophysiol 82:18081817.
Buonomano DV (2000) Decoding temporal information: a model based on short-term synaptic plasticity. J Neurosci 20:11291141.
Chance FS, Nelson SB, Abbott LF (1999) Complex cells as cortically amplified simple cells. Nat Neurosci 2:277282.[CrossRef][ISI][Medline]
Chapin JK (1986) Laminar differences in sizes, shapes, and response profiles of cutaneous receptive fields in the rat SI cortex. Exp Brain Res 62:549559.[ISI][Medline]
Clarey JC, Barone P, Imig TJ (1992) Physiology of thalamus and cortex. In: The mammalian auditory pathway: neurophysiology (Popper E, Fay R, eds), pp. 232334. New York: Springer-Verlag.
Clarey JC, Barone P, Imig TJ (1994) Functional organization of sound direction and sound pressure level in primary auditory cortex of the cat. J Neurophysiol 72:23832405.
Connors BW, Gutnick MJ (1990) Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13:99104.[CrossRef][ISI][Medline]
Cruikshank SJ, Rose HJ, Metherate R (2002) Auditory thalamocortical synaptic transmission in vitro. J Neurophysiol 87:361384.
Daw NW, Fox K, Sato H, Czepita D (1992) Critical period for monocular deprivation in the cat visual cortex. J Neurophysiol 67:197202.
Dear SP, Fritz J, Haresign T, Ferragamo M, Simmons JA (1993) Tonotopic and functional organization in the auditory cortex of the big brown bat, Eptesicus fuscus. J Neurophysiol 70:19882009.
DeFelipe J, Conley M, Jones EG (1986) Long-range focal collateralization of axons arising from corticocortical cells in monkey sensory-motor cortex. J Neurosci 6:37493766.[Abstract]
Desai NS, Cudmore RH, Nelson SB, Turrigiano GG (2002) Critical periods for experience-dependent synaptic scaling in visual cortex. Nat Neurosci 5:783789.[ISI][Medline]
Diamond ME, Huang W, Ebner FF (1994) Laminar comparison of somatosensory cortical plasticity. Science 265:18851888.[ISI][Medline]
DiCarlo J, Johnson K (2002) Receptive field structure in cortical area 3b of the alert monkey. Behav Brain Res 135:167178.[CrossRef][ISI][Medline]
Eggermont JJ (1996) How homogeneous is cat primary auditory cortex? Evidence from simultaneous single-unit recordings. Aud Neurosci 2:7996.[ISI]
Foeller E, Vater M, Kossl M (2001) Laminar analysis of inhibition in the gerbil primary auditory cortex. J Assoc Res Otolaryngol 2:279296.[Medline]
Gilbert CD (1977) Laminar differences in receptive field properties of cells in cat primary visual cortex. J Physiol 268:391421.[ISI][Medline]
Gilbert CD, Wiesel TN (1979) Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280:120125.[ISI][Medline]
Hefti BJ, Smith PH (2000) Anatomy, physiology, and synaptic responses of rat layer V auditory cortical cells and effects of intracellular GABA(A) blockade. J Neurophysiol 83:26262638.
Hefti BJ, Smith PH (2002) Distribution and kinetic properties of GABAergic inputs to layer V pyramidal cells in rat auditory cortex. J Assoc Res Otolayrngol DOI: 10.1007/s10162-002-3012-z.
Hirsch JA, Alonso JM, Reid RC, Martinez LM (1998) Synaptic integration in striate cortical simple cells. J Neurosci 18:95179528.
Huang CL, Winer JA (2000) Auditory thalamocortical projections in the cat: laminar and areal patterns of input. J Comp Neurol 427:302331.[CrossRef][ISI][Medline]
Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cats visual cortex. J Physiol (Lond) 160:106154.[ISI][Medline]
Hübener M, Shoham D, Grinvald A, Bonhoeffer T (1997) Spatial relationship among three columnar systems in cat area 17. J Neurosci 17:92709784.
Imig TJ, Adrián HO (1977) Binaural columns in the primary field (A1) of cat auditory cortex. Brain Res 138:241257.[CrossRef][ISI][Medline]
Imig TJ, Brugge JF (1978) Sources and terminations of callosal axons related to binaural and frequency maps in primary auditory cortex of the cat. J Comp Neurol 182:637660.[ISI][Medline]
Innocenti GM (1980) The primary visual pathway through the corpus callosum: morphological and functional aspects in the cat. Arch Ital Biol 118:124188.[ISI][Medline]
Innocenti GM (1986) General organization of callosal connections in the cerebral cortex. In: Cerebral cortex (Jones EG, Peters A, eds), Vol. 5, pp. 291353. New York: Plenum Press.
Jen PH, Sun XD, Lin PJ (1989) Frequency and space representation in the primary auditory cortex of the frequency modulating bat Eptesicus fuscus. J Comp Neurol A 165:114.
Jones EG (1975) Varieties and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J Comp Neurol 160:205267.[ISI][Medline]
Jones EG (2002) Microcolumns in the cerebral cortex. Proc Natl Acad Sci USA 97:50195021.
Kilgard MP, Pandya PK, Vazquez J, Gehi A, Schreiner CE, Merzenich MM (2001) Sensory input directs spatial and temporal plasticity in primary auditory cortex. J Neurophysiol 86:326338.
Kral A, Hartmann R, Tillein J, Heid S, Klinke R (2000) Congenital auditory deprivation reduces synaptic activity within the auditory cortex in a layer-specific manner. Cereb Cortex 10: 714726.
Landry P, Deschênes M (1981) Intracortical arborizations and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat. J Comp Neurol 199:345371.[ISI][Medline]
LeVay S, Gilbert CD (1976) Laminar patterns of geniculocortical projection in the cat. Brain Res 113:119.[CrossRef][ISI][Medline]
Linden JF, Liu RC, Sahani M, Schreiner CE, Merzenich MM (2002) Spectrotemporal structure of receptive fields in areas AI and AAF of mouse auditory cortex. Soc Neurosci Abstr 32:458.4.
Lund JS, Henry GH, MacQueen CL, Harvey AR (1979) Anatomical organization of the primary visual cortex (area 17) in the cat. A comparison with are 17 of the macaque monkey. J Comp Neurol 184:599618.[ISI][Medline]
Mangini NJ, Pearlman AL (1980) Laminar distribution of receptive field properties in the primary visual cortex of the mouse. J Comp Neurol 193:203222.[ISI][Medline]
Manzoni T, Barbaresi P, Bellardinelli E, Caminiti R (1980) Callosal projections from the two body midlines. Exp Brain Res 39:19.[ISI][Medline]
Martinez LM, Alonso JM (2001) Construction of complex receptive fields in cat primary visual cortex. Neuron 32:515525.[CrossRef][ISI][Medline]
Martinez LM, Alonso JM, Reid RC, Hirsch JA (2002) Laminar processing of stimulus orientation in cat visual cortex. J Physiol 540:321333.
Matsubara JA, Phillips DP (1988) Intracortical connections and their physiological correlates in the primary auditory cortex (AI) of the cat. J Comp Neurol 268:3848.[ISI][Medline]
McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782806.
Mel BW, Ruderman DL, Archie KA (1998) Translation-invariant orientation tuning in visual complex cells could derive from intradendritic computations. J Neurosci 18:43254334.
Mendelson JR, Schreiner CE, Sutter ML, Grasse KL (1993) Functional topography of cat primary auditory cortex: responses to frequency-modulated sweeps. Exp Brain Res 94:6587.[ISI][Medline]
Mendelson JR, Schreiner CE, Sutter ML (1997) Functional topography of cat primary auditory cortex: response latencies. J Comp Physiol A 181:615633.[ISI][Medline]
Merzenich MM, Knight PL, Roth GL (1975) Representation of the cochlea within primary auditory cortex in the cat. J Neurophysiol 38:231249.
Metherate R, Aramakis VB (1999) Intrinsic electrophysiology of neurons in thalamorecipient layers of developing rat auditory cortex. Brain Res Dev Brain Res 115:131144.[ISI][Medline]
Métin C, Godement P, Imbert M (1988) The primary visual cortex in the mouse: receptive field properties and functional organization. Exp Brain Res 69:594612.[ISI][Medline]
Middlebrooks JC, Dykes RW, Merzenich MM (1980) Binaural response-specific bands in primary auditory cortex (AI) of the cat: topographical organization orthogonal to isofrequency contours. Brain Res 181:3148.[CrossRef][ISI][Medline]
Miller LM, Escabí MA, Read HL, Schreiner CE (2001) Functional convergence of response properties in the auditory thalamocortical system. Neuron 32:151160.[ISI][Medline]
Mitani A, Shimokouchi M (1985) Neuronal connections in the primary auditory cortex: an electrophysiological study in the cat. J Comp Neurol 235:417429.[ISI][Medline]
Mitani A, Shimokouchi M, Itoh K, Nomura S, Kudo M, Mizuno N (1985) Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat. J Comp Neurol 235:430447.[ISI][Medline]
Ojima H, Honda CN, Jones EG (1991) Patterns of axon collateralization of identified supragranular pyramidal neurons in the cat auditory cortex. Cereb Cortex 1:8094.[Abstract]
Oonishi S, Katsuki Y (1965) Functional organization and integrative mechanisms on the auditory cortex of the cat. Japan J Physiol 15:342365.[ISI]
Phillips DP, Irvine DRF (1981) Responses of single neurons in physiologically defined primary auditory cortex (AI) of the cat: frequency tuning and responses to intensity. J Neurophysiol 45:4858.
Phillips DP, Irvine DRF (1983) Some features of binaural input to single neurons in physiologically defined area AI of cat cerebral cortex. J Neurophysiol 49:383395.
Pinto DJ, Brumberg JC, Simons DJ (2000) Circuit dynamics and coding strategies in rodent somatosensory cortex. J Neurophysiol 83:11581166.
Read HL, Winer JA, Schreiner CE (2001) Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex. Proc Natl Acad Sci USA 98:80428047.
Recanzone GH, Schreiner CE, Merzenich MM (1993) Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J Neurosci 13:87103.[Abstract]
Reid RC, Alonso JM (1995) Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378:281284.[CrossRef][ISI][Medline]
Reser DH, Fishman YI, Arezzo JC, Steinschneider M (2000) Binaural interactions in primary auditory cortex of the awake macaque. Cereb Cortex 10:574584.
Ringach DL, Shapley RM, Hawken MJ (2002) Orientation selectivity in macaque V1: diversity and laminar dependence. J Neurosci 22:56395651.
Rockel AJ, Hiorns RW, Powell TPS (1980) The basic uniformity in the structure of the neocortex. Brain 103:221244.[ISI][Medline]
Rockland KS, Lund JS (1983) Intrinsic laminar lattice connections in primate visual cortex. J Comp Neurol 216:303318.[ISI][Medline]
Roe AW, Pallas SL, Hahm JO, Sur M (1990) A map of visual space induced in primary auditory cortex. Science 250:818820.[ISI][Medline]
Roe AW, Pallas SL, Kwon YH, Sur M (1992) Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex. J Neurosci 12:36513664.[Abstract]
Sahani M, Linden JF (2002) Evidence optimization techniques for estimating stimulus-response functions. In: Advances in neural information processing systems (Becker S, Than S, Obermeyer K, eds), Vol. 15. Cambridge, MA: MIT Press (in press).
Schreiner CE, Mendelson JR (1990) Functional topography of cat primary auditory cortex: distribution of integrated excitation. J Neurophysiol 64:14421459.
Schreiner CE, Read HL, Sutter ML (2000) Modular organization of frequency integration in primary auditory cortex. Annu Rev Neurosci 23:501529.[CrossRef][ISI][Medline]
Schwark HD, Jones EG (1989) The distribution of intrinsic cortical axons in area 3b of cat primary somatosensory cortex. Exp Brain Res 78:501513.[ISI][Medline]
Sharma J, Angelucci A, Sur M (2000) Induction of visual orientation modules in auditory cortex. Nature 404:841847.[CrossRef][ISI][Medline]
Shen JX, Xu ZM, Yao YD (1999) Evidence for columnar organization in the auditory cortex of the mouse. Hear Res 137:174177.[CrossRef][ISI][Medline]
Simons DJ (1978) Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophys 41:798820.
Simons DJ, Carvell GE (1989) Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol 61:311330.
Simons DJ, Woolsey TA (1984) Morphology of Golgi-Cox-impregnated barrel neurons in rat SmI cortex. J Comp Neurol 230:119132.[ISI][Medline]
Smith PH, Populin LC (2001) Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices. J Comp Neurol 436:508519.[CrossRef][ISI][Medline]
Somers DC, Nelson SB, Sur M (1995) An emergent model of orientation selectivity in cat visual cortical simple cells. J Neurosci 15:54485465.[Abstract]
Sretavan D, Dykes RW (1983) The organization of two cutaneous submodalities in the forearm region of area 3b of cat somatosensory cortex. J Comp Neurol 13:381398.
Stern EA, Maravall M, Svoboda K (2001) Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo. Neuron 31:305315.[CrossRef][ISI][Medline]
Suga N (1965) Functional properties of auditory neurones in the cortex of echo-locating bats. J Physiol (Lond) 181:671700.[ISI][Medline]
Sugimoto S, Sakurada M, Horikawa J, Taniguchi I (1997) The columnar and layer-specific response properties of neurons in the primary auditory cortex of Mongolian gerbils. Hear Res 112:175185.[CrossRef][ISI][Medline]
Sur M, Wall JT, Kaas JH (1984) Modular distribution of neurons with slowly adapting and rapidly adapting responses in area 3b of somatosensory cortex in monkeys. J Neurophysiol 51: 724744.
Sur M, Garraghty PE, Bruce CJ (1985) Somatosensory cortex in macaque monkeys: laminar differences in receptive field size in areas 3b and 1. Brain Res 342:391395.[CrossRef][ISI][Medline]
Sur M, Garraghty PE, Roe AW (1988) Experimentally induced visual projections into auditory thalamus and cortex. Science 242:14371441.[ISI][Medline]
Sutter ML, Schreiner CE (1991) Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. J Neurophysiol 65:12071226.
Swadlow HA, Gusev AG (2000) The influence of single VB thalamocortical impulses on barrel columns of rabbit somatosensory cortex. J Neurophysiol 83:28022813.
Swadlow HA, Gusev AG (2002) Receptive-field construction in cortical inhibitory interneurons. Nat Neurosci 5:403404.[CrossRef][ISI][Medline]
Trachtenberg JT, Trepel C, Stryker MP (2000) Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. Science 287:20292032.
Troyer TW, Krukowski AE, Priebe NJ, Miller KD (1998) Contrastinvariant orientation tuning in cat visual cortex: thalamocortical input tuning and correlation-based intracortical connectivity. J Neurosci 18:59085927.
Wallace MN, Kitzes LM, Jones EG (1991) Intrinsic inter- and intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex. Exp Brain Res 86:527544.[ISI][Medline]
Weinberger NM (1998) Physiological memory in primary auditory cortex: characteristics and mechanisms. Neurobiol Learn Mem 70:226251.[CrossRef][ISI][Medline]
Winer JA (1992) The functional architecture of the medial geniculate body and the primary auditory cortex. In: The mammalian auditory pathway: neuroanatomy (Webster DB, Popper AN, Fay RR, eds), pp. 222409. New York: Springer-Verlag.
Zhang LI, Bao S, Merzenich MM (2001) Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat Neurosci 4:11231130.[CrossRef][ISI][Medline]