F. de Ribaupierre

Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas

SummaryThe origin and laminar arrangement of the homolateral and callosal projections to the anterior (AAF), primary (AI), posterior (PAF) and secondary (AII) auditory cortical areas were studied in the cat by means of electrophysiological recording and WGA-HRP tracing techniques. The transcallosal projections to AAF, AI, PAF and AII were principally homotypic since the major source of input was their corresponding area in the contralateral cortex. Heterotypic transcallosal projections to AAF and AI were seen, originating from the contralateral AI and AAF, respectively. PAF received heterotypic commissural projections from the opposite ventroposterior auditory cortical field (VPAF). Heterotypic callosal inputs to AII were rare, originating from AAF and AI. The neurons of origin of the transcallosal connections were located mainly in layers II and III (70–92%), and less frequently in deep layers (V and VI, 8–30%). Single unit recordings provided evidence that both homotypic and heterotypic transcallosal projections connect corresponding frequency regions of the two hemispheres. The regional distribution of the anterogradely labeled terminals indicated that the homotypic and heterotypic auditory transcallosal projections are reciprocal. The present data suggest that the transcallosal auditory interconnections are segregated in 3 major parallel components (AAF-AI, PAF-VPAF and AII), maintaining a segregation between parallel functional channels already established for the thalamocortical auditory interconnections. For the intrahemispheric connections, the analysis of the retrograde tracing data revealed that AAF and AI receive projections from the homolateral cortical areas PAF, VPAF and AII, whose neurons of origin were located mainly in their deep (V and VI) cortical layers. The reciprocal interconnections between the homolateral AAF and AI did not show a preferential laminar arrangement since the neurons of origin were distributed almost evenly in both superficial (II and III) and deep (V and VI) cortical layers. On the contrary, PAF received inputs from the homolateral cortical fields AAF, AI, AII and VPAF, originating predominantly from their superficial (II and III) layers. The homolateral projections reaching AII originated mainly from the superficial layers of AAF and AI, but from the deep layers of VPAF and PAF. The laminar distribution of anterogradely labeled terminal fields, when they were dense enough for a confident identification, was systematically related to the laminar arrangement of neurons of origin of the reciprocal projection: a projection originating from deep layers was associated with a reciprocal projection terminating mainly in layer IV, whereas a projection originating from superficial layers was associated with a reciprocal projection terminating predominantly outside layer IV. This laminar distribution indicates that the homolateral auditory cortical interconnections have a feed-forward/feed-back organization, corresponding to a hierarchical arrangement of the auditory cortical areas, according to criteria previously established in the visual system of primates. The principal auditory cortical areas could be ranked into 4 distinct hierarchical levels. The tonotopically organized areas AAF and AI represent the lowest level. The second level corresponds to the non-tonotopically organized area AII. Higher, the tonotopically organized areas VPAF and PAF occupy the third and fourth hierarchical levels, respectively.

Corticofugal modulation of the information processing in the auditory thalamus of the cat

SummarySingle unit activity of 355 cells was recorded in the auditory thalamus of anesthetized cats before, during, and after the inactivation by cooling of the ipsilateral primary auditory cortex (AI). Most of the units (n = 288) showed similar functional characteristics of firing before and after the cryogenic blockade of AI. The spontaneous firing rate remained unchanged by cooling in 20% of the units and decreased in the majority of them (60%). In some regions, i.e. dorsal division of the medial geniculate body (MGB), lateral part of the posterior group of the thalamus, and auditory sector of the reticular nucleus of the thalamus, the maximum firing rate evoked by white noise bursts was generally affected by cooling in the same direction and to the same extent as the spontaneous activity. Units in the ventral division of MGB showed a characteristic increase of signal-to-noise ratio during cortical cooling. The corticofugal modulation led to the appearance or disappearance of the best frequency of tuning in 51 units and changed it by more than 0.5 octave in 34 units. The bandwidths of different response patterns to pure tones stimulation were used to define a set of functional properties. During cryogenic blockade of AI, two cortically modulated sub-populations of units were usually distinguished that exhibited changes for a given functional property. The complexity and diversity of the effects of cortical inactivation suggest that the corticothalamic projection may be the support for selective operations such as an adaptive filtering of the incoming acoustic signal at the thalamic level adjusted as a function of cortical activity.

Functional organization of the ventral division of the medial geniculate body of the cat: Evidence for a rostro-caudal gradient of response properties and cortical projections

The response properties to clicks, noise and tone bursts of 2152 single units located in the ventral division of the medial geniculate body were analysed as a function of their anatomical position. A particular spatial distribution of these properties was observed in the pars lateralis (LV) and ovoidea (OV). The distribution of different response characteristics changed along the rostro-caudal axis. Units located posteriorly were in majority either insensitive to simple acoustical stimuli or responded exclusively to pure tones, presenting generally a broad tuning and a loose tonotopic arrangement. Inhibitory response patterns were about as frequent as excitatory ones, response latencies were long on the average and widely distributed. Only a few units showed time-locking of their discharges in response to repetitive clicks. Most units had non-monotonic intensity functions. Going anteriorly, the distribution of response properties progressively changed: the number of units sensitive to various simple acoustical stimuli (pure tones and broad band stimuli together) increased, the tonotopic arrangement was more precise and more units were sharply tuned. Response patterns were in majority of the excitatory type, and latencies were shorter on the average and less dispersed. More units were precisely time-locked to repetitive clicks. The proportion of units with monotonic intensity functions increased. The origin of thalamo-cortical projections was studied with focal injections of wheat-germ agglutinin labeled with horseradish peroxidase in functionally defined loci of the various auditory cortical fields. An evolution of the density of labeled cells in LV and OV was observed along the same rostro-caudal axis for which a gradient of functional properties is described above. Thalamo-cortical projections to the primary auditory area and the anterior auditory field originated predominantly from the anterior half of LV, whereas the posterior auditory field received inputs from a wider rostro-caudal extend of LV including its posterior half.

Functional organization of the medial division of the medial geniculate body of the cat: Tonotopic organization, spatial distribution of response properties and cortical connections

The discharge properties of 735 single units located in the pars magnocellularis (M) of the medial division of the medial geniculate body (MGB) were studied in 23 nitrous oxide anesthetized cats in response to simple acoustic stimuli (clicks, noise and tone bursts). A systematic decrease of single unit characteristic frequencies (CF) was observed along electrode track portions crossing M from dorso-medial to ventro-lateral. These data indicate that M is tonotopically organized with an arrangement of low CF units latero-ventrally and high CF units dorso-medially. This preferential arrangement of single units as a function of their CF was consistent with the location and orientation of clusters of labeled cells in M resulting from wheat-germ agglutinin labeled with horseradish peroxidase (WGA-HRP) injections in CF defined loci in the anterior (AAF) or primary (AI) auditory cortical fields. The quality of the tonotopic arrangement was low caudally and increased in the rostral direction, indicating that this tonotopicity concerns mainly the anterior half of M. Response latencies to clicks, noise and tone bursts were on average longer in the posterior part of M than in its anterior part. Time-locking of discharges in response to repetitive acoustic pulses was more frequent anteriorly than posteriorly and the upper limiting rate of locking was on average higher rostrally (up to 200-300 Hz). In contrast, other response properties such as responsiveness to the various combinations of simple acoustic stimuli, response patterns and tuning were more randomly distributed in M, showing the whole range of response properties seen in the MGB. Data derived from several injections of WGA-HRP performed in distinct auditory cortical fields in several animals indicated that M projects to the tonotopic cortical fields (AAF, AI and PAF) as well as to the non-tonotopically organized secondary auditory cortex (AII). The contribution of M to the total thalamic input reaching each field of the auditory cortex was quantitatively more important for AAF (30%) and PAF (20%) than for AI and AII (about 10% each).

Phase-locked responses to low frequency tones in the medial geniculate body

Abstract Over 2500 extracellular single unit recordings were obtained from the medial geniculate body (MGB) of cats anaesthetized with nitrous oxide. Three out of four units were activated by tone bursts, most of them presenting a transient ‘on’ response. Only about 10% of the units showed a sustained excitatory ‘through’ response. Some of these neurons, when activated by low-frequency tone bursts, had discharge synchronized with the phase of the tonal stimulus. Such phase-locked units were principally found in the pars lateralls, but also in the pars magnocellularis and pars ovoidea of the MGB. Significant phase-locking (vector strength R ⩾ 0.5) was observed up to 1000 Hz. About 20% of all units, responding in a sustained fashion to tone bursts below that frequency, were phase-locked. Monaural stimulation led to a shift of the mean phase angle compared to that measured when the tone bursts were delivered simultaneously to both ears. Implications of these experimental results on the synaptic jitter and the information processing through the auditory pathways are discussed.

Tonotopic organization in the medial geniculate body (MGB) of lightly anesthetized cats

SummaryIn the medial geniculate body (MGB) of nitrous oxide anesthetized cats, the pars lateralis (PL) was the only nucleus to show a clear topographic arrangement of its neurons according to their characteristic frequency (CF). When compared to barbiturate anesthetized cats (Imig and Morel 1985a), the tonotopic organization in PL appeared less strict and was characterized by a significant local CF disparity. Furthermore, the degree of tonotopic organization varied along the rostrocaudal axis of the nucleus: it was lower in its caudal than in its rostral half. In the pars ovoidea, the rostral half of the pars magnocellularis (PM) and the suprageniculate nucleus, CF sequences and quantitative evaluations of the tonotopicity indicated the presence of some degree of tonotopic organization which was lower than in PL. No such organization was observed in the caudal part of PM nor in the ventrolateral nucleus, while in the dorsal nucleus, the proportion of toneresponding units was too low for a significant analysis.

Origin of afferents to physiologically defined regions of the medial geniculate body of the cat: ventral and dorsal divisions.

To study the origin of afferents to the medial geniculate body (MGB), single unit recordings were first conducted to define physiologically a given region in this auditory thalamic nucleus. Horseradish peroxidase (HRP) was then injected extracellularly, in order to label retrogradely the neurons whose axon terminals end in this region. The principal inputs to the MGB are coming from various nuclei of the brain stem, the auditory cortex and the reticular complex of the thalamus. The ventral division receives its cortical inputs principally from the primary (AI) and the posterior (PAF) auditory cortical fields, with a quantitatively smaller contribution of the secondary (AII) and anterior (AAF) cortical fields. On the other hand, the dorsal division receives a majority of its cortical inputs from AII, with a less important contribution of AI and PAF. The auditory cortex sends roughly as many axons to these two divisions as does the brain stem, mainly the inferior colliculus (IC). The analysis of ascending inputs to the same regions of the MGB reveals that, on the average, 88%, 7% and 5% of them are coming from the ipsilateral IC, the contralateral IC and other nuclei of the brain stem, respectively.

Neurons sensitive to narrow ranges of repetitive acoustic transients in the medial geniculate body of the cat

SummaryNeuronal activity was recorded in the medial geniculate body (MGB) of nitrous oxide anaesthetized, paralysed cats in response to click trains. For most cells responding to these stimuli the spike discharges are precisely time locked to individual clicks within the train. The present study has revealed that, apart from the normal “locker” response being characterized by a monotonic decrease in the entrainment as the frequency of the clicks within the train increases, there is a small population of “lockers” which show a non-monotonic response to increasing click frequency. 41% of these non-monotonic cells were not at all entrained by the lowest click rates and had time-locked responses for very restricted frequency ranges. These particular non-monotonic “lockers” were more commonly-found in the posterior part of the pars lateralis and in the suprageniculate nucleus. These cells might be involved in the temporal coding of natural sounds such as animal vocalizations and the cats purr.

Transmission delay of phase-locked cells in the medial geniculate body

Over 4000 single unit recordings were obtained from the medial geniculate body (MGB) of nitrous oxide anaesthetized cats. Out of 1600 cells sensitive to tone bursts below 4 kHz, 10% were responding in a sustained manner. From these, 121 were tested for phase-locked responses. The general characteristics of these units have been described in a previous report. The central tendency of the discharges distribution within the period or mean phase angle was studied for many frequencies in 24 phase-locked units. For each of them, the mean phase angle shifts linearly with the frequency. The slope of these phase versus frequency lines is an accurate measure of the transmission delay from the cochlea to the MGB. This delay is a function of the units characteristic frequency and shows that the time spread introduced by the cochlea between the high and low frequency components of an acoustic signal is preserved up to the MGB. Subtracting the cochlear delay from this overall delay, the neural delay from the eighth nerve to the MGB was found to be 6.4 ms for neurons having a CF above 300 Hz; it was greater by 3 ms for cells with a CF below that frequency.

Interconnections of the auditory cortical fields of the cat with the cingulate and parahippocampal cortices

SummaryThe interconnections of the auditory cortex with the parahippocampal and cingulate cortices were studied in the cat. Injections of the anterograde and retrograde tracer WGA-HRP were performed, in different cats (n = 9), in electrophysiologically identified auditory cortical fields. Injections in the posterior zone of the auditory cortex (PAF or at the PAF/AI border) labeled neurons and axonal terminal fields in the cingulate gyrus, mainly in the ventral bank of the splenial sulcus (a region that can be considered as an extension of the cytoarchitectonic area Cg), and posteriorly in the retrosplenial area. Labeling was also present in area 35 of the perirhinal cortex, but it was sparser than in the cingulate gyrus. Following WGA-HRP injection in All, no labeling was found in the cingulate gyrus, but a few neurons and terminals were labeled in area 35. In contrast, no or very sparse labeling was observed in the cingulate and perirhinal cortices after WGA-HRP injections in the anterior zone of the auditory cortex (AI or AAF). A WGA-HRP injection in the cingulate gyrus labeled neurons in the posterior zone of the auditory cortex, between the posterior ectosylvian and the posterior suprasylvian sulci, but none was found more anteriorly in regions corresponding to AI, AAF and AII. The present data indicate the existence of preferential interconnections between the posterior auditory cortex and the limbic system (cingulate and parahippocampal cortices). This specialization of posterior auditory cortical areas can be related to previous observations indicating that the anterior and posterior regions of the auditory cortex differ from each other by their response properties to sounds and their pattern of connectivity with the auditory thalamus and the claustrum.