Gregg H. Recanzone

Temporal and spatial dependency of the ventriloquism effect.

The perception of the spatial location of an auditory stimulus can be captured by a spatially disparate visual stimulus, a phenomenon known as the ventriloquism effect. This study investigated the temporal and spatial dependency of this illusion. In the temporal domain, only disparities of 50–100 ms were perceived as simultaneous, and disparities where the visual stimulus occurred before the auditory stimulus were more effective in creating the illusion. In the spatial domain, the illusion was elicited most strongly at spatial disparities below spatial discrimination thresholds. There was also a significant interaction between temporal and spatial disparities. These results indicate that both temporal and spatial parameters are critical in the perception of real world objects in extrapersonal space.

Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys

To gain insight into how cortical fields process somatic inputs and ultimately contribute to complex abilities such as tactile object perception, we examined the pattern of connections of two areas in the lateral sulcus of macaque monkeys: the second somatosensory area (S2), and the parietal ventral area (PV). Neuroanatomical tracers were injected into electrophysiologically and/or architectonically defined locations, and labeled cell bodies were identified in cortex ipsilateral and contralateral to the injection site. Transported tracer was related to architectonically defined boundaries so that the full complement of connections of S2 and PV could be appreciated. Our results indicate that S2 is densely interconnected with the primary somatosensory area (3b), PV, and area 7b of the ipsilateral hemisphere, and with S2, 7b, and 3b in the opposite hemisphere. PV is interconnected with areas 3b and 7b, with the parietal rostroventral area, premotor cortex, posterior parietal cortex, and with the medial auditory belt areas. Contralateral connections were restricted to PV in the opposite hemisphere. These data indicate that S2 and PV have unique and overlapping patterns of connections, and that they comprise part of a network that processes both cutaneous and proprioceptive inputs necessary for tactile discrimination and recognition. Although more data are needed, these patterns of interconnections of cortical fields and thalamic nuclei suggest that the somatosensory system may not be segregated into two separate streams of information processing, as has been hypothesized for the visual system. Rather, some fields may be involved in a variety of functions that require motor and sensory integration. J. Comp. Neurol. 462:382–399, 2003.

Response profiles of auditory cortical neurons to tones and noise in behaving macaque monkeys

The primate auditory cortex is anatomically divided into several areas, but little is known about the functional differences between these areas. Similarly, although neurons in sub-cortical auditory areas of other species have been classified into distinct categories, these criteria have not been applied in primates. This study measured the responses of single neurons in the primary auditory cortex (AI) and the caudomedial field (CM) to tones and noise. Most neurons could be qualitatively classified as onset, sustained, or sustained-onset, but never as primary (VIII nerve)-like or chopper. Quantitative analysis showed a continuum of response types, from having only onset responses to responding throughout the stimulus period. AI neurons had higher firing rates that CM neurons, but CM neurons had higher firing rates to noise stimuli compared to tone stimuli, and a greater percentage of CM neurons had excitatory responses after stimulus offset. There were no differences in the percentage of neurons that had tonic or inhibitory responses. These results indicate that the responses of neurons in the primate auditory cortex are better described as a continuum rather than as discrete classes, and provide further evidence that auditory information is processed in series between AI and CM in the primate.

Functional Organization of Spectral Receptive Fields in the Primary Auditory Cortex of the Owl Monkey

Recent experiments in the cat have demonstrated that several response parameters, including frequency tuning, intensity tuning, and FM selectivity, are spatially segregated across the isofrequency axis. To investigate whether a similar functional organization exists in the primate, we have studied the spatial distribution of pure‐tone receptive field parameters across the primary auditory cortex (AI) in six owl monkeys (Aotus trivirgatus). The distributions of binaural interaction types and onset latency were also examined. Consistent with previous studies, the primary auditory cortex contained a clear cochleotopic organization. We demonstrate here that several other properties of the responses to tonal stimuli also showed nonrandom spatial distributions that were largely independent from each other. In particular, the sharpness of frequency tuning to pure tones, intensity tuning and sensitivity, response latency, and binaural interaction types all showed spatial variations that were independent from the representation of characteristic frequency and from each other. Statistical analysis confirmed that these organizations did not reflect random distributions. The overall organizational pattern of overlaying but independent functional maps that emerged was quite similar to that seen in AI of cats and, in general, appears to reflect a fundamental organization principle of primary sensory cortical fields. J. Comp. Neurol. 415:460–481, 1999.

Populations of auditory cortical neurons can accurately encode acoustic space across stimulus intensity

The auditory cortex is critical for perceiving a sounds location. However, there is no topographic representation of acoustic space, and individual auditory cortical neurons are often broadly tuned to stimulus location. It thus remains unclear how acoustic space is represented in the mammalian cerebral cortex and how it could contribute to sound localization. This report tests whether the firing rates of populations of neurons in different auditory cortical fields in the macaque monkey carry sufficient information to account for horizontal sound localization ability. We applied an optimal neural decoding technique, based on maximum likelihood estimation, to populations of neurons from 6 different cortical fields encompassing core and belt areas. We found that the firing rate of neurons in the caudolateral area contain enough information to account for sound localization ability, but neurons in other tested core and belt cortical areas do not. These results provide a detailed and plausible population model of how acoustic space could be represented in the primate cerebral cortex and support a dual stream processing model of auditory cortical processing.

Organization of area 3a in macaque monkeys: Contributions to the cortical phenotype

The detailed organization of somatosensory area 3a was examined in macaque monkeys using multiunit electrophysiological recording techniques. By examining topographic relationships, changes in receptive field size, and the type of stimulus that neurons responded to, functional boundaries of area 3a were determined and related to architectonic boundaries. One striking observation was that the location of area 3a varied with respect to the central sulcus. In one‐half of the cases area 3a was on the rostral bank and fundus of the central sulcus and in the other half of the cases it was on the caudal bank and fundus of the central sulcus. In terms of topographic organization, we found that area 3a contains a complete representation of deep receptors and musculature of the contralateral body, and that the general organization of body part representations mirrors that of the primary somatosensory area, 3b. These results as well as results from studies of area 3a in ours and other laboratories indicate that area 3a is part of a network involved in proprioception, postural control, and the generation of coordinated movements. Further, comparative analysis of area 3a in a variety of species suggests that its construction is based, to a large extent, on the use of a particular body part rather than on innervation density. J. Comp. Neurol. 471:97–111, 2004.

Interactions of Auditory and Visual Stimuli in Space and Time

The nervous system has evolved to transduce different types of environmental energy independently, for example light energy is transduced by the retina whereas sound energy is transduced by the cochlea. However, the neural processing of this energy is necessarily combined, resulting in a unified percept of a real-world object or event. These percepts can be modified in the laboratory, resulting in illusions that can be used to probe how multisensory integration occurs. This paper reviews studies that have utilized such illusory percepts in order to better understand the integration of auditory and visual signals in primates. Results from human psychophysical experiments where visual stimuli alter the perception of acoustic space (the ventriloquism effect) are discussed, as are experiments probing the underlying cortical mechanisms of this integration. Similar psychophysical experiments where auditory stimuli alter the perception of visual temporal processing are also described.

Representation of Con-Specific Vocalizations in the Core and Belt Areas of the Auditory Cortex in the Alert Macaque Monkey

Auditory cortical processing in primates has been proposed to be divided into two parallel processing streams, a caudal spatial stream and a rostral nonspatial stream. Previous single neuron studies have indicated that neurons in the rostral lateral belt respond selectively to vocalization stimuli, whereas imaging studies have indicated that selective vocalization processing first occurs in higher order cortical areas. To test the dual stream hypothesis and to find evidence to account for the difference between the electrophysiological and imaging results, we recorded the responses of single neurons in core and belt auditory cortical fields to both forward and reversed vocalizations. We found that there was little difference in the overall firing rate of neurons across different cortical areas or between forward and reversed vocalizations. However, more information was carried in the overall firing rate for forward vocalizations compared with reversed vocalizations in all areas except the rostral field of the core (area R). These results are consistent with the imaging results and are inconsistent with early rostral cortical areas being involved in selectively processing vocalization stimuli based on a firing rate code. They further suggest that a more complex processing scheme is in play in these early auditory cortical areas.

Alterations in correlated activity parallel ICMS-induced representational plasticity

We studied neural interactions by cross correlation analysis during representational plasticity induced by intracortical microstimulation (ICMS). Neuron pairs were simultaneously recorded in area 3b in adult New World monkeys, and in cortical field SI in adult rats. In normal animals, the degree of correlated spontaneous activity corresponded to the extent of receptive field overlap. After several hours of ICMS, the spatial extents of cortex over which correlated activity could be recorded was enlarged several-fold. Mapping experiments revealed that increased correlated activity was only recorded within that cortical sector that was representationally reorganized, indicating a close relationship between cortical reorganization and cooperative processes. Results support the hypothesis that discharge coincidence is crucial for the formation of functionally coupled neural groups, and implicate dynamically maintained groups in the genesis of postontogenetic plasticity.

Visually Induced Plasticity of Auditory Spatial Perception in Macaques

When experiencing spatially disparate visual and auditory stimuli, a common percept is that the sound originates from the location of the visual stimulus, an illusion known as the ventriloquism effect. This illusion can persist for tens of minutes, a phenomenon termed the ventriloquism aftereffect. The underlying neuronal mechanisms of this rapidly induced plasticity remain unclear; indeed, it remains untested whether similar multimodal interactions occur in other species. We therefore tested whether macaque monkeys experience the ventriloquism aftereffect similar to the way humans do. The ability of two monkeys to determine which side of the midline a sound was presented from was tested before and after a period of 20-60 min in which the monkeys experienced either spatially identical or spatially disparate auditory and visual stimuli. In agreement with human studies, the monkeys did experience a shift in their auditory spatial perception in the direction of the spatially disparate visual stimulus, and the aftereffect did not transfer across sounds that differed in frequency by two octaves. These results show that macaque monkeys experience the ventriloquism aftereffect similar to the way humans do in all tested respects, indicating that these multimodal interactions are a basic phenomenon of the central nervous system.