The distributed auditory cortex

Abstract

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.

Fig. 1

Some basic anatomical features of cat auditory cortex (AC) area AI (primary AC). (A) Major cell types include glutamatergic pyramidal cells (1–3), GABAergic basket (4) and multipolar (5) neurons, spinous inverted pyramidal cells (6), bipolar cells (7), small multipolar neurons (8), and horizontal cells in layers I (9) and VI (10). Many more subtypes are found in morphological studies limited largely to AI (Winer, 1992). Golgi-Cox impregnation, 140 μm thick section, planachromat, N.A. 0.95, ×1000. (B) AI cytoarchitecture shows a prominent layer I, a dense concentration of layer II cells, smaller layer IV cells, and columnar somatic arrangements in deeper layers. Nissl preparation, 30 μm thick celloidin embedded section, planapochromat, N.A. 0.65, ×500. (C–E) Laminar distribution of thalamocortical boutons after medial geniculate body (MGB) deposits of biotinylated dextran amines (Huang and Winer, 2000). Abscissa, bouton percentages/layer in pia-white matter traverses. (C) After ventral division tracer deposits, labeling is concentrated in layer III. (D) MGB dorsal division deposits had a wider laminar dispersion. (E) Medial division deposits had a bilaminar AC pattern. (F) The proportion of γ-aminobutyric acid-containing (GABAergic) AI cells is lamina specific. Antisera to GABA, 30 μm thick frozen section (Prieto et al., 1994b). (G) The laminar origins of six AI projection systems (1–6). While these origins overlap, few such neurons project to multiple subcortical targets (Wong and Kelly, 1981); gray background, intrinsic and local projections (Read et al., 2001), also present within the colored regions. 1: unpublished observations; 2: Code and Winer (1985); 3: Winer and Prieto (2001); 4: Winer (2005); 5: Schofield and Coomes (2004); 6: Schofield and Coomes (2005). For abbreviations, see the list.

Fig. 2

AC extrinsic connections. Ascending (A–C) and descending (H–M) projections. (A) The areal distribution of thalamocortical axons is widespread (Huang and Winer, 2000). (B) Ipsilateral corticocortical long range projections suggest that the tonotopic areas (AI, AAF, P, VP, Ve) are a group, that the non-primary areas (AII, AES, DZ) have a wide range of weaker inputs which largely exclude multisensory and limbic sources; and that limbic (In, Te) and multisensory areas (ED, EI, EV) are independent of the tonotopic areas and have mutual and reciprocal inputs with one another (unpublished observations). (C) The commissural projections are smaller and more reciprocal than those of the corticocortical system (unpublished observations). (D) Cat AC areas (Lee and Winer, 2005). (E) Cat basal forebrain subdivisions (Beneyto and Prieto, 2001). (F) Cat MGB subdivisions (Winer, 1992). (G) Cat inferior colliculus subdivisions (Winer, 2005). (H) Corticothalamic projections are as specific and focal as thalamocortical projections (A) (Winer et al., 2001). (I) Corticocollicular projections show modest central nucleus input and non-primary AC projections as topographic as those of the primary areas (Winer et al., 1998). (J) Central gray input arises largely from multisensory and non-primary AC (Winer et al., 1998). (K) Corticostriatal and corticoamygdaloid input is as specific as that of the corticothalamic streams (Beneyto and Prieto, 2001). (L) Rodent corticoolivary (Schofield and Coomes, 2004) and (M) corticocochlear projections (Schofield and Coomes, 2005) are target-specific.

Fig. 3

The distributed AC and its extrinsic relations. (A) The ascending (black) and descending (blue) auditory systems. (B) The multimodal limb targets primarily non-tonotopic AC areas (Bowman and Olson, 1988a), which are linked to tonotopic areas via corticocortical input (Bowman and Olson, 1988b). Vestibular and somatic sensory influence reaches MGB subdivisions (Blum et al., 1979) which project widely to AC and beyond (Winer and Morest, 1983). (C) The premotor relations with nigral, striatal, and paralemniscal areas might coordinate skeletal (Olazábal and Moore, 1989) and smooth muscle (Winer, 2006) and vocalization-related pathways (Feliciano et al., 1995) in auditory and multimodal behaviors. (D) The plasticity-associated limb is related to nucleus basalis (NB/SI) input to AC (Kamke et al., 2005). Perirhinal cortex targets both MGB (chiefly non-lemniscal) and AC (all areas) extensively (Witter and Groenewegen, 1986). (E) The AC input to the amygdala (Al) and central gray (CG) allows access to many extraauditory sites (Clascá et al., 2000). (F) In the macaque, convergent input to the prefrontal cortex may represent parallel acoustic object recognition and localization streams, respectively (Rauschecker and Tian, 2000); frontal lobe influence likewise reaches wide expanses of the supratemporal plane (Jones and Powell, 1970). Input from the multimodal suprageniculate nucleus (Sl) to the frontal lobe (?) is of unknown significance (Kobler et al., 1987). Relations with the thalamic reticular nucleus (Crabtree, 1998) and the effects of ventral tegmental stimulation on AC plasticity (Bao et al., 2001) have been omitted for reasons of space. See text for discussion.