Jeffery A. Winer

Auditory cortical projections to the cat inferior colliculus

The projection from 11 auditory cortical areas onto the subdivisions of the inferior colliculus was studied in adult cats by using two different anterograde tracers to label corticocollicular (CC) axon terminals. The main results were that: 1) a significant CC projection arose from every field; 2) the principal inferior collicular targets were the dorsal cortex, lateral nucleus, caudal cortex, and intercollicular tegmentum, with only a sparse projection to the central nucleus; 3) the input was usually bilateral, with the ipsilateral side by far the most heavily labeled, and the contralateral projection was a symmetrical subset of the ipsilateral input; 4) the CC system is both divergent and convergent, with single cortical areas projecting to six or more collicular subdivisions, and each auditory midbrain subdivision receiving a convergent projection from two to ten cortical areas; 5) cortical areas devoid of tonotopic organization have topographic projections to collicular target nuclei; 6) the heaviest CC projection terminated in the caudal half of the inferior colliculus; and finally, 7) the relative strength of the corticocollicular labeling was far less than that of the corresponding corticothalamic projection in the same experiments.

Decoding the auditory corticofugal systems

The status of the organization of the auditory corticofugal systems is summarized. These are among the largest pathways in the brain, with descending connections to auditory and non-auditory thalamic, midbrain, and medullary regions. Auditory corticofugal influence thus reaches sites immediately presynaptic to the cortex, sites remote from the cortex, as in periolivary regions that may have a centrifugal role, and to the cochlear nucleus, which could influence early central events in hearing. Other targets include the striatum (possible premotor functions), the amygdala and central gray (prospective limbic and motivational roles), and the pontine nuclei (for precerebellar control). The size, specificity, laminar origins, and morphologic diversity of auditory corticofugal axons is consonant with an interpretation of multiple roles in parallel descending systems.

Auditory thalamocortical projections in the cat: Laminar and areal patterns of input

Thalamocortical projections were studied in adult cats using biotinylated dextran amines, wheat germ agglutinin conjugated to horseradish peroxidase, and autoradiography with tritiated leucine and/or proline. The input from 7 architectonically defined nuclei to 14 auditory cortical fields was characterized qualitatively and quantitatively. The principal results were that 1) every thalamic nucleus projected to more than 1 field (range, 4–14 fields; mean, 7 fields); 2) only the projection from the ventral division to some primary fields (primary auditory cortex and posterior auditory cortex) had a periodic, clustered distribution, whereas the input from other divisions to nonprimary areas was continuous; 3) layers III–V received >85% of the total axonal profiles; 4) in most experiments, five or more layers were labeled; 5) the projections to nonprimary auditory areas had many laterally oriented axons; 6) the heaviest input to layer I in all experiments was usually in its upper half, suggesting a sublaminar arrangement; 7) the largest axonal trunks (up to 6 μm in diameter) arose from the medial division and ended in layer Ia, where they ran laterally for long distances; 8) there were three projection patterns: type 1 had its peak in layers III–IV with little input to layer I, and it arose from the ventral division and the dorsal superficial, dorsal, and suprageniculate nuclei of the dorsal division; type 2 had heavy labeling in layer I and less in layers III–IV, arising from the dorsal division nuclei primarily, especially the caudal dorsal and deep dorsal nuclei; and type 3 was a trimodal concentration in layers I, III–IV, and VI that originated chiefly in the medial division and had the lowest density of labeling; and 9) the quantitative profiles with the three methods were very similar. The results suggest that the subdivisions of the auditory thalamus have consistent patterns of laminar distribution to different cortical areas, that an average of five or more layers receive significant input in a specific area, that a given thalamic nucleus can influence areas as far as 20 mm apart, that the first information to arrive at the cortex may reach layer I by virtue of the giant axons, and that several laminar patterns of auditory thalamocortical projection exist. The view that the auditory thalamus (and perhaps other thalamic nuclei) serves mainly a relay function underestimates its many modes for influencing the cortex on a laminar basis. J. Comp. Neurol. 427:302–331, 2000.

Auditory Cortex Mapmaking: Principles, Projections, and Plasticity

Maps of sensory receptor epithelia and computed features of the sensory environment are common elements of auditory, visual, and somatic sensory representations from the periphery to the cerebral cortex. Maps enhance the understanding of normal neural organization and its modification by pathology and experience. They underlie the derivation of the computational principles that govern sensory processing and the generation of perception. Despite their intuitive explanatory power, the functions of and rules for organizing maps and their plasticity are not well understood. Some puzzles of auditory cortical map organization are that few complete receptor maps are available and that even fewer computational maps are known beyond primary cortical areas. Neuroanatomical evidence suggests equally organized connectional patterns throughout the cortical hierarchy that might underlie map stability. Here, we consider the implications of auditory cortical map organization and its plasticity and evaluate the complementary role of maps in representation and computation from an auditory perspective.

Auditory thalamocortical transformation: structure and function

Communicative, predatory, and reproductive behaviors rely on the auditory thalamocortical system, a key nexus that combines, transforms, and distributes virtually all acoustic information relevant to survival. The rules of connectivity for this complex network, both anatomically and functionally, are only beginning to be uncovered. Although the auditory thalamocortical system shares many features with other modalities, its connectivity and information processing principles differ from those of other modalities in many ways. Some physiological and anatomical bases for these differences are the subject of this review.

Layer V in rat auditory cortex: Projections to the inferior colliculus and contralateral cortex

This study compares the form and distribution within layer V of cells projecting to the inferior colliculus with that of commissural cells of origin in adult rat auditory cortex after horseradish peroxidase injections in the ipsilateral inferior colliculus or auditory cortex. The goal of this work was to determine whether every part of layer V participates equally in both projections, and if the cortical neurons in each pathway were similar. The types of neurons were defined in Golgi-Cox preparations and matched with the profiles of retrogradely labeled cells from architectonically defined cortical area 41. Inferior colliculus and commissural neurons form two populations that differ in their distribution in layer V, in somatic area, and in the form of their apical dendritic arbors. Corticocollicular neurons include the largest pyramidal cells, whose robustly filled apical dendrites ascend into layer II or farther. Commissural cells are smaller and have a more heterogeneous form. Their apical dendrites do not usually extend above layer IV, and a few of these cells may be non-pyramidal. Small pyramidal cells and inverted pyramidal cells project to the opposite cortex, but not to the inferior colliculus. Medium-sized pyramidal cells project in both systems. In addition, certain callosal cells of origin in layers V and III were morphologically similar. More than one-third of the commissural cells originate in the superficial part of layer V, where only 7% of the inferior colliculus projection neurons arise. Most corticocollicular cells lie deeper in layer V, where there are fewer commissural neurons. These findings suggest that the efferent systems projecting to telencephalic and mesencephalic targets are morphologically distinct and spatially segregated in layer V. However, the commissural projection includes similar cells in different cortical layers. The types of these efferent neurons may be more closely related to their target than to their laminar origin.

Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex

Many response properties in primary auditory cortex (AI) are segregated spatially and organized topographically as those in primary visual cortex. Intensive study has not revealed an intrinsic, anatomical organizing principle related to an AI functional topography. We used retrograde anatomic tracing and topographic physiologic mapping of acoustic response properties to reveal long-range (≥1.5 mm) convergent intrinsic horizontal connections between AI subregions with similar bandwidth and characteristic frequency selectivity. This suggests a modular organization for processing spectral bandwidth in AI.

Projections of Auditory Cortex to the Medial Geniculate Body of the Cat

The corticofugal projection from 12 auditory cortical fields onto the medial geniculate body was investigated in adult cats by using wheat germ agglutinin conjugated to horseradish peroxidase or biotinylated dextran amines. The chief goals were to determine the degree of divergence from single cortical fields, the pattern of convergence from several fields onto a single nucleus, the extent of reciprocal relations between corticothalamic and thalamocortical connections, and to contrast and compare the patterns of auditory corticogeniculate projections with corticofugal input to the inferior colliculus. The main findings were that (1) single areas showed a wide range of divergence, projecting to as few as 5, and to as many as 15, thalamic nuclei; (2) most nuclei received projections from approximately five cortical areas, whereas others were the target of as few as three areas; (3) there was global corticothalamic‐thalamocortical reciprocity in every experiment, and there were also significant instances of nonreciprocal projections, with the corticothalamic input often more extensive; (4) the corticothalamic projection was far stronger and more divergent than the corticocollicular projection from the same areas, suggesting that the thalamus and the inferior colliculus receive differential degrees of corticofugal control; (5) cochleotopically organized areas had fewer corticothalamic projections than fields in which tonotopy was not a primary feature; and (6) all corticothalamic projections were topographic, focal, and clustered, indicating that areas with limited cochleotopic organization still have some internal spatial arrangement. The areas with the most divergent corticothalamic projections were polysensory regions in the posterior ectosylvian gyrus. The projection patterns were indistinguishable for the two tracers. These findings suggest that every auditory thalamic nucleus is under some degree of descending control. Many of the projections preserve the relations between cochleotopically organized thalamic and auditory areas, and suggest topographic relations between nontonotopic areas and nuclei. The collective size of the corticothalamic system suggests that both lemniscal and extralemniscal auditory thalamic nuclei receive significant corticofugal input. J. Comp. Neurol. 430:27–55, 2001.

The distributed auditory cortex.

A synthesis of cat auditory cortex (AC) organization is presented in which the extrinsic and intrinsic connections interact to derive a unified profile of the auditory stream and use it to direct and modify cortical and subcortical information flow. Thus, the thalamocortical input provides essential sensory information about peripheral stimulus events, which AC redirects locally for feature extraction, and then conveys to parallel auditory, multisensory, premotor, limbic, and cognitive centers for further analysis. The corticofugal output influences areas as remote as the pons and the cochlear nucleus, structures whose effects upon AC are entirely indirect, and it has diverse roles in the transmission of information through the medial geniculate body and inferior colliculus. The distributed AC is thus construed as a functional network in which the auditory percept is assembled for subsequent redistribution in sensory, premotor, and cognitive streams contingent on the derived interpretation of the acoustic events. The confluence of auditory and multisensory streams likely precedes cognitive processing of sound. The distributed AC constitutes the largest and arguably the most complete representation of the auditory world. Many facets of this scheme may apply in rodent and primate AC as well. We propose that the distributed auditory cortex contributes to local processing regimes in regions as disparate as the frontal pole and the cochlear nucleus to construct the acoustic percept.

The medial geniculate body of the cat.

1 Introduction.- 2 Materials and Methods.- 3 Observations.- 4 Discussion.- 5 Summary.- 6 Acknowledgements.- 7 References.