LANGUAGE DEVELOPMENT. The developmental dynamics of marmoset monkey vocal production.

Human vocal development occurs through two parallel interactive processes that transform infant cries into more mature vocalizations, such as cooing sounds and babbling. First, natural categories of sounds change as the vocal apparatus matures. Second, parental vocal feedback sensitizes infants to certain features of those sounds, and the sounds are modified accordingly. Paradoxically, our closest living ancestors, nonhuman primates, are thought to undergo few or no production-related acoustic changes during development, and any such changes are thought to be impervious to social feedback. Using early and dense sampling, quantitative tracking of acoustic changes, and biomechanical modeling, we showed that vocalizations in infant marmoset monkeys undergo dramatic changes that cannot be solely attributed to simple consequences of growth. Using parental interaction experiments, we found that contingent parental feedback influences the rate of vocal development. These findings overturn decades-old ideas about primate vocalizations and show that marmoset monkeys are a compelling model system for early vocal development in humans.

The auditory behaviour of primates: a neuroethological perspective.

The ethological approach has already provided rich insights into the auditory neurobiology of a number of different taxa (e.g. birds, frogs and insects). Understanding the ethology of primates is likely to yield similar insights into the specializations of this taxa's auditory system for processing species-specific vocalisations. Here, we review the recent advances made in our understanding of primate vocal perception and its neural basis.

Role of cortical feedback in the receptive field structure and nonlinear response properties of somatosensory thalamic neurons.

Previous studies have suggested that the descending pathway from the primary somatosensory (SI) cortex to the ventral posterior nucleus of the thalamus has only a mild facilitative influence over thalamic neurons. Given the large numbers of corticothalamic terminations within the rat somatosensory thalamus and their complex topography, we sought to examine the role of corticothalamic feedback in the genesis of spatiotemporal receptive fields and the integration of complex tactile stimuli in the thalamus. By combining focal cortical inactivation (produced by microinjection of the GABA(A) agonist muscimol), with chronic multielectrode recordings, we observed that feedback from the rat SI cortex has multiple influences on its primary thalamic relay, the ventral posterior medial (VPM) nucleus. Our data demonstrate that, when single-whisker stimuli were used, the elimination of cortical feedback caused significant changes in the spatiotemporal structure of the receptive fields of VPM neurons. Cortical feedback also accounted for the nonlinear summation of VPM neural responses to simultaneously stimulated whiskers, in effect "linearizing" the responses. These results argue that the integration and transmission of tactile information through VPM are strongly influenced by the state of SI cortex.

The units of perception in the antiphonal calling behavior of cotton-top tamarins (Saguinus oedipus): playback experiments with long calls.

We investigated how the acoustic structure of the cotton-top tamarin monkey's (Saguinus oedipus) combination long call relates to the antiphonal calling behavior of conspecifics. Combination long calls can function as contact calls and are produced by socially isolated individuals. Often conspecifics respond to these calls with their own long calls. Structurally, these calls are always composed of one or more 'chirps' followed by two or more 'whistles'. We compared the antiphonal calling responses to playbacks of complete, naturally produced long calls versus single whistles or single chirps. Subjects responded significantly more to whole calls than to either syllable-type alone. Thus, our data suggest that, in terms of the antiphonal calling behavior of socially isolated conspecifics, the whole long call is the unit of perception.

Feature article: the structure and function of dynamic cortical and thalamic receptive fields.

Under natural conditions, animals must process spatiotemporally complex signals in order to guide adaptive behavior. It follows that the response properties of neurons should reflect the dynamic nature of such signals. Recently, several studies have demonstrated the existence of time-varying receptive fields in the auditory, visual and somatosensory thalamocortical pathways. The characteristics of these receptive fields suggest that they are constrained by the need to actively interpret time-varying stimuli. Here, we review these studies, the possible functions of these receptive fields, and how they might be generated in the thalamocortical pathway.

The role of temporal cues in rhesus monkey vocal recognition: orienting asymmetries to reversed calls.

An understanding of the acoustic cues that animals use to categorize their vocalizations has important implications for the way we design neuroethological investigations of auditory function. Compared to other species, we know relatively little about the kinds of acoustic features used by nonhuman primates to recognize and categorize vocalizations. To further our understanding, this study explores the role of temporal features in recognition of conspecific vocalizations by rhesus macaques (Macaca mulatta). Experiments were designed to extend an earlier set of findings showing that adult rhesus macaques selectively turn with the right ear leading when a conspecific vocalization is played 180 degrees behind them, but turn left or not at all when a non-conspecific signal is played. Two call types were used as stimuli: shrill barks (alarm call) and harmonic arches (food call). We found that for normal calls, rhesus macaques turned to the right - supporting earlier findings - but for time- reversed shrill barks and harmonic arches, subjects oriented to the left. These results suggest that for at least a subset of calls, rhesus macaques use temporal cues to recognize conspecific vocal signals. The asymmetry of the behavioral response, and the corresponding asymmetry in the time-amplitude waveform, may have important implications for studies of temporal coding in the primate auditory system.

Encoding of tactile stimulus location by somatosensory thalamocortical ensembles.

The exquisite modular anatomy of the rat somatosensory system makes it an excellent model to test the potential coding strategies used to discriminate the location of a tactile stimulus. Here, we investigated how ensembles of simultaneously recorded single neurons in layer V of primary somatosensory (SI) cortex and in the ventral posterior medial (VPM) nucleus of the thalamus of the anesthetized rat may encode the location of a single whisker stimulus on a single trial basis. An artificial neural network based on a learning vector quantization algorithm, was used to identify putative coding mechanisms. Our data suggest that these neural ensembles may rely on a distributed coding scheme to represent the location of single whisker stimuli. Within this scheme, the temporal modulation of neural ensemble firing rate, as well as the temporal interactions between neurons, contributed significantly to the representation of stimulus location. The relative contribution of these temporal codes increased with the number of whiskers that the ensembles must discriminate among. Our results also indicated that the SI cortex and the VPM nucleus may function as a single entity to encode stimulus location. Overall, our data suggest that the representation of somatosensory features in the rat trigeminal system may arise from the interactions of neurons within and between the SI cortex and VPM nucleus. Furthermore, multiple coding strategies may be used simultaneously to represent the location of tactile stimuli.

Spatiotemporal properties of layer V neurons of the rat primary somatosensory cortex.

Animals in their natural environments actively process spatiotemporally complex sensory signals in order to guide adaptive behavior. It therefore seems likely that the properties of both single neurons and neural ensembles should reflect the dynamic nature of such interactions. During exploratory behaviors, rats move their whiskers to actively discriminate between different tactile features. We investigated whether this dynamic sensory processing was reflected in the spatial and temporal properties of neurons in layer V of the 'whisker area' in the rat primary somatosensory cortex. We found that the majority of layer V neurons had large (8.5+/-4.9 whiskers) spatiotemporal receptive fields (i.e. individual cells responded best to different whiskers as a function of post-stimulus time), and that the excitatory responses of surround whiskers formed a spatial gradient of excitation that seemed to reflect the greater use of the ventral and caudal whiskers during natural behaviors. Analyses of ensembles of layer V neurons revealed that single-whisker stimuli activated a portion of layer V that extends well beyond a single cortical column (average of 5.6 barrel cortical columns). Based on these results, we conclude that the rat primary somatosensory cortex does not appear to operate as a static decoder of tactile information. On the contrary, our data suggest that tactile processing in rats is likely to involve the on-going interactions between populations of broadly tuned neurons in the thalamocortical pathway.

Immediate thalamic sensory plasticity depends on corticothalamic feedback.

Multiple neuron ensemble recordings were obtained simultaneously from both the primary somatosensory (SI) cortex and the ventroposterior medial thalamus (VPM) before and during the combined administration of reversible inactivation of the SI cortex and a reversible subcutaneous block of peripheral trigeminal nerve fibers. This procedure was performed to quantify the contribution of descending corticofugal projections on (i) the normal organization of thalamic somatosensory receptive fields and (ii) the thalamic somatosensory plastic reorganization that immediately follows a peripheral deafferentation. Reversible inactivation of SI cortex resulted in immediate changes in receptive field properties throughout the VPM. Cortical inactivation also significantly reduced but did not completely eliminate the occurrence of VPM receptive field reorganization resulting from the reversible peripheral deafferentation. This result suggests that the thalamic plasticity that is seen immediately after a peripheral deafferentation is dependent upon both descending corticofugal projections and ascending trigeminothalamic projections.

The effects of estradiol on gonadotropin-releasing hormone neurons in the developing mouse brain.

The hypothalamic-pituitary-gonadal (HPG) axis plays a critical role in the control of reproduction. Two key hormonal components of the HPG axis are gonadal steroids and gonadotropin-releasing hormone (GnRH). Gonadal steroids are known to organize the development of neural substrates which control adult reproductive behavior; GnRH is required for normal reproductive structure and function. The possibility that gonadal steroids may produce organizational changes in the pattern of GnRH staining observed in the brain is investigated through the use of injections of estradiol to neonatal mice and subsequent GnRH immunocytochemistry at 2 months of age. Our results indicate that the number of GnRH-immunoreactive (GnRH-ir) cells is normally lower in females than males. Estradiol did not affect the number of GnRH-ir cells in females, but significantly increased the number of GnRH-ir cells in males, suggesting that early exposure to estradiol results in masculinization of the GnRH axis of males.

Simultaneous encoding of tactile information by three primate cortical areas.

We used simultaneous multi-site neural ensemble recordings to investigate the representation of tactile information in three areas of the primate somatosensory cortex (areas 3b, SII and 2). Small neural ensembles (30-40 neurons) of broadly tuned somatosensory neurons were able to identify correctly the location of a single tactile stimulus on a single trial, almost simultaneously. Furthermore, each of these cortical areas could use different combinations of encoding strategies, such as mean firing rate (areas 3b and 2) or temporal patterns of ensemble firing (area SII), to represent the location of a tactile stimulus. Based on these results, we propose that ensembles of broadly tuned neurons, located in three distinct areas of the primate somatosensory cortex, obtain information about the location of a tactile stimulus almost concurrently.

Nonlinear processing of tactile information in the thalamocortical loop.

Rats explore tangible objects in a manner such that, at any given moment in time, multiple facial whiskers simultaneously contact the surface of the object. Although both thalamic and cortical neurons responsible for processing such tactile information have large, multiwhisker receptive fields, it remains unclear what kinds of computations can be carried out by these neuronal populations when behaviorally relevant multiwhisker stimuli are used. By simultaneously recording the activity of up to 78 cortical and thalamic neurons per animal, we observed that the magnitude of sensory responses and the spatial spread of ensemble activity increased in a nonlinear fashion according to the extent and spatial orientation of the multiwhisker stimuli. Supralinear responses were seen more frequently with vertically than with horizontally oriented stimuli. These data suggest that thalamocortical interactions in the rat somatosensory system can generate complex spatial transformations of multiwhisker stimuli that go beyond the classic inhibitory interactions previously observed.

Reconstructing the engram: simultaneous, multisite, many single neuron recordings.

Little is known about the physiological principles that govern large-scale neuronal interactions in the mammalian brain. Here, we describe an electrophysiological paradigm capable of simultaneously recording the extracellular activity of large populations of single neurons, distributed across multiple cortical and subcortical structures in behaving and anesthetized animals. Up to 100 neurons were simultaneously recorded after 48 microwires were implanted in the brain stem, thalamus, and somatosensory cortex of rats. Overall, 86% of the implanted microwires yielded single neurons, and an average of 2.3 neurons were discriminated per microwire. Our population recordings remained stable for weeks, demonstrating that this method can be employed to investigate the dynamic and distributed neuronal ensemble interactions that underlie processes such as sensory perception, motor control, and sensorimotor learning in freely behaving animals.