Faculty Bibliography

Our working model of the primate auditory cortex recognizes three major regions (core, belt, parabelt), subdivided into thirteen areas. The connections between areas are topographically ordered in a manner consistent with information flow along two major anatomical axes: core-belt-parabelt and caudal-rostral. Remarkably, most of the connections supporting this model were revealed using retrograde tracing techniques. Little is known about laminar circuitry, as anterograde tracing of axon terminations has rarely been used. The purpose of the present study was to examine the laminar projections of three areas of auditory cortex, pursuant to analysis of all areas. The selected areas were: middle lateral belt (ML); caudomedial belt (CM); and caudal parabelt (CPB). Injections of anterograde tracers yielded data consistent with major features of our model, and also new findings that compel modifications. Results supporting the model were: (1) feedforward projection from ML and CM terminated in CPB; (2) feedforward projections from ML and CPB terminated in rostral areas of the belt and parabelt; and (3) feedback projections typified inputs to the core region from belt and parabelt. At odds with the model was the convergence of feedforward inputs into rostral medial belt from ML and CPB. This was unexpected since CPB is at a higher stage of the processing hierarchy, with mainly feedback projections to all other belt areas. Lastly, extending the model, feedforward projections from CM, ML, and CPB overlapped in the temporal parietal occipital area (TPO) in the superior temporal sulcus, indicating significant auditory influence on sensory processing in this region. The combined results refine our working model and highlight the need to complete studies of the laminar inputs to all areas of auditory cortex. Their documentation is essential for developing informed hypotheses about the neurophysiological influences of inputs to each layer and area.

The current working model of primate auditory cortex is constructed from a number of studies of both new and old world monkeys. It includes three levels of processing. A primary level, the core region, is surrounded both medially and laterally by a secondary belt region. A third level of processing, the parabelt region, is located lateral to the belt. The marmoset monkey (Callithrix jacchus jacchus) has become an important model system to study auditory processing, but its anatomical organization has not been fully established. In previous studies, we focused on the architecture and connections of the core and medial belt areas (de la Mothe et al., 2006a, J Comp Neurol 496:27-71; de la Mothe et al., 2006b, J Comp Neurol 496:72-96). In this study, the corticocortical connections of the lateral belt and parabelt were examined in the marmoset. Tracers were injected into both rostral and caudal portions of the lateral belt and parabelt. Both regions revealed topographic connections along the rostrocaudal axis, where caudal areas of injection had stronger connections with caudal areas, and rostral areas of injection with rostral areas. The lateral belt had strong connections with the core, belt, and parabelt, whereas the parabelt had strong connections with the belt but not the core. Label in the core from injections in the parabelt was significantly reduced or absent, consistent with the idea that the parabelt relies mainly on the belt for its cortical input. In addition, the present and previous studies indicate hierarchical principles of anatomical organization in the marmoset that are consistent with those observed in other primates.

The primate auditory cortex is comprised of a core region of three primary areas, surrounded by a belt region of secondary areas and a parabelt region lateral to the belt. The main sources of thalamocortical inputs to the auditory cortex are the medial geniculate complex (MGC), medial pulvinar (PM), and several adjoining nuclei in the posterior thalamus. The distribution of inputs varies topographically by cortical area and thalamic nucleus, but in a manner that has not been fully characterized in primates. In this study, the thalamocortical connections of the lateral belt and parabelt were determined by placing retrograde tracer injections into various areas of these regions in the marmoset monkey. Both regions received projections from the medial (MGm) and posterodorsal (MGpd) divisions of the medial geniculate complex (MGC); however, labeled cells in the anterodorsal (MGad) division were present only from injections into the caudal belt. Thalamic inputs to the lateral belt appeared to come mainly from the MGC, whereas the parabelt also received a strong projection from the PM, consistent with its position as a later stage of auditory cortical processing. The results of this study also indicate that the organization of the marmoset auditory cortex is similar to other primates.

Local field potentials (LFPs) are of growing importance in neurophysiological investigations. LFPs supplement action potential recordings by indexing activity relevant to EEG, magnetoencephalographic, and hemodynamic (fMRI) signals. Recent reports suggest that LFPs reflect activity within very small domains of several hundred micrometers. We examined this conclusion by comparing LFP, current source density (CSD), and multiunit activity (MUA) signals in macaque auditory cortex. Estimated by frequency tuning bandwidths, these signals' "listening areas" differ systematically with an order of MUA < CSD < LFP. Computational analyses confirm that observed LFPs receive local contributions. Direct measurements indicate passive spread of LFPs to sites more than a centimeter from their origins. These findings appear to be independent of the frequency content of the LFP. Our results challenge the idea that LFP recordings typically integrate over extremely circumscribed local domains. Rather, LFPs appear as a mixture of local potentials with "volume conducted" potentials from distant sites.

We examined multiunit responses to tones and to 1/3 and 2/3 octave band-pass noise (BPN) in the marmoset primary auditory cortex (A1) and the caudomedial belt (CM). In both areas, BPN was more effective than tones, evoking multiunit responses at lower intensity and across a wider frequency range. Typically, the best responses to BPN remained at the characteristic frequency. Additionally, in both areas responses to BPN tended to be of greater magnitude and shorter latency than responses to tones. These effects are consistent with the integration of more excitatory inputs driven by BPN than by tones. While it is generally thought that single units in A1 prefer narrow band sounds such as tones, we found that best responses for multi units in both A1 and CM were obtained with noises of narrow spectral bandwidths.

The primate auditory cortex contains three interconnected regions (core, belt, parabelt), which are further subdivided into discrete areas. The caudomedial area (CM) is one of about seven areas in the belt region that has been the subject of recent anatomical and physiological studies conducted to define the functional organization of auditory cortex. The main goal of the present study was to examine temporal coding in area CM of marmoset monkeys using two related classes of acoustic stimuli: (1) marmoset twitter calls; and (2) frequency-modulated (FM) sweep trains modeled after the twitter call. The FM sweep trains were presented at repetition rates between 1 and 24 Hz, overlapping the natural phrase frequency of the twitter call (6-8 Hz). Multiunit recordings in CM revealed robust phase-locked responses to twitter calls and FM sweep trains. For the latter, phase-locking quantified by vector strength (VS) was best at repetition rates between 2 and 8 Hz, with a mean of about 5 Hz. Temporal response patterns were not strictly phase-locked, but exhibited dynamic features that varied with the repetition rate. To examine these properties, classification of the repetition rate from the temporal response pattern evoked by twitter calls and FM sweep trains was examined by Fisher's linear discrimination analysis (LDA). Response classification by LDA revealed that information was encoded not only by phase-locking, but also other components of the temporal response pattern. For FM sweep trains, classification was best for repetition rates from 2 to 8 Hz. Thus, the majority of neurons in CM can accurately encode the envelopes of temporally complex stimuli over the behaviorally-relevant range of the twitter call. This suggests that CM could be engaged in processing that requires relatively precise temporal envelope discrimination, and supports the hypothesis that CM is positioned at an early stage of processing in the auditory cortex of primates.

It is widely recognized that viewing a speaker's face enhances vocal communication, although the neural substrates of this phenomenon remain unknown. We propose that the enhancement effect uses the ongoing oscillatory activity of local neuronal ensembles in the primary auditory cortex. Neuronal oscillations reflect rhythmic shifting of neuronal ensembles between high and low excitability states. Our hypothesis holds that oscillations are 'predictively' modulated by visual input, so that related auditory input arrives during a high excitability phase and is thus amplified. We discuss the anatomical substrates and key timing parameters that enable and constrain this effect. Our hypothesis makes testable predictions for future studies and emphasizes the idea that 'background' oscillatory activity is instrumental to cortical sensory processing.

The auditory cortex of primates contains a core region of three primary areas surrounded by a belt region of secondary areas. Recent neurophysiological studies suggest that the belt areas medial to the core have unique functional roles, including multisensory properties, but little is known about their connections. In this study and its companion, the cortical and subcortical connections of the core and medial belt regions of marmoset monkeys were compared to account for functional differences between areas and refine our working model of the primate auditory cortex. Anatomical tracer injections targeted two core areas (A1 and R) and two medial belt areas (rostromedial [RM] and caudomedial [CM]). RM and CM had topographically weighted connections with all other areas of the auditory cortex ipsilaterally, but these were less widespread contralaterally. CM was densely connected with caudal auditory fields, the retroinsular (Ri) area of the somatosensory cortex, the superior temporal sulcus (STS), and the posterior parietal and entorhinal cortex. The connections of RM favored rostral auditory areas, with no clear somatosensory inputs. RM also projected to the lateral nucleus of the amygdala and tail of the caudate nucleus. A1 and R had topographically weighted connections with medial and lateral belt regions, infragranular inputs from the parabelt, and weak connections with fields outside the auditory cortex. The results indicated that RM and CM are distinct areas of the medial belt region with direct inputs from the core. CM also has somatosensory input and may correspond to an area on the posteromedial transverse gyrus of humans and the anterior auditory field of other mammals.

In this study and its companion, the cortical and subcortical connections of the medial belt region of the marmoset monkey auditory cortex were compared with the core region. The main objective was to document anatomical features that account for functional differences observed between areas. Injections of retrograde and bi-directional anatomical tracers targeted two core areas (A1 and R), and two medial belt areas (rostromedial [RM] and caudomedial [CM]). Topographically distinct patterns of connections were revealed among subdivisions of the medial geniculate complex (MGC) and multisensory thalamic nuclei, including the suprageniculate (Sg), limitans (Lim), medial pulvinar (PM), and posterior nucleus (Po). The dominant thalamic projection to the CM was the anterior dorsal division (MGad) of the MGC, whereas the posterior dorsal division (MGpd) targeted RM. CM also had substantial input from multisensory nuclei, especially the magnocellular division (MGm) of the MGC. RM had weak multisensory connections. Corticotectal projections of both RM and CM targeted the dorsomedial quadrant of the inferior colliculus, whereas the CM projection also included a pericentral extension around the ventromedial and lateral portion of the central nucleus. Areas A1 and R were characterized by focal topographic connections within the ventral division (MGv) of the MGC, reflecting the tonotopic organization of both core areas. The results indicate that parallel subcortical pathways target the core and medial belt regions and that RM and CM represent functionally distinct areas within the medial belt auditory cortex.