Traditional cortical parcellation schemes have emphasized the presence of sharply defined visual, auditory, and somatosensory domains populated exclusively by modality-specific neurons (i.e., neurons responsive to sensory stimuli from a single sensory modality). However, the modality-exclusivity of this scheme has recently been challenged. Observations in a variety of species suggest that each of these domains is subject to influences from other senses. Using the cerebral cortex of the rat as a model, the present study systematically examined the capability of individual neurons in visual, auditory, and somatosensory cortex to be activated by stimuli from other senses. Within the major modalityspecific domains, the incidence of inappropriate (i.e., nonmatching) and͞or multisensory neurons was very low. However, at the borders between each of these domains a concentration of multisensory neurons was found whose modality profile matched the representations in neighboring cortices and that were able to integrate their cross-modal inputs to give rise to enhanced and͞or depressed responses. The results of these studies are consistent with some features of both the traditional and challenging views of cortical organization, and they suggest a parcellation scheme in which modality-specific cortical domains are separated from one another by transitional multisensory zones.
This study proposes a classification system for neurons in the central nucleus of the inferior colliculus (ICC) that is based on excitation and inhibition patterns of single-unit responses in decerebrate cats. The decerebrate preparation allowed extensive characterization of physiological response types without the confounding effects of anesthesia. The tone-driven discharge rates of individual units were measured across a range of frequencies and levels to map excitatory and inhibitory response areas for contralateral monaural stimulation. The resulting frequency response maps can be grouped into the following three populations: type V maps exhibit a wide V-shaped excitatory area and no inhibition; type I maps show a more restricted I-shaped region of excitation that is flanked by inhibition at lower and higher frequencies; and type O maps display an O-shaped island of excitation at low stimulus levels that is bounded by inhibition at higher levels. Units that produce a type V map typically have a low best frequency (BF: the most sensitive frequency), a low rate of spontaneous activity, and monotonic rate-level functions for both BF tones and broadband noise. Type I and type O units have BFs that span the cat's range of audible frequencies and high rates of spontaneous activity. Like type V units, type I units are excited by BF tones and noise at all levels, but their rate-level functions may become nonmonotonic at high levels. Type O units are inhibited by BF tones and noise at high levels. The existence of distinct response types is consistent with a conceptual model in which the unit types receive dominant inputs from different sources and shows that these functionally segregated pathways are specialized to play complementary roles in the processing of auditory information.
Single neuron studies provide one foundation for understanding many facets of multisensory integration. These studies have used a variety of criteria for identifying and quantifying multisensory integration. While a number of techniques have been used, there lacks an explicit discussion of the assumptions, criteria, and analytical methods traditionally used to define the principles of multisensory integration. This was not problematic when the field was small, but with rapid growth a number of alternative techniques and models have been introduced, each with its own criteria and sets of implicit assumptions to define and characterize what is thought to be the same phenomenon. The potential for misconception prompted this reexamination of traditional approaches in order to clarify their underlying assumptions and analytic techniques. The objective is to review the traditional quantitative methods advanced in the study of single-neuron physiology in order to appreciate the process of multisensory integration and its impact.
Cochlear synaptopathy can result from various insults, including acoustic trauma, aging, ototoxicity, or chronic conductive hearing loss. For example, moderate noise exposure in mice can destroy up to ∼50% of synapses between auditory nerve fibers (ANFs) and inner hair cells (IHCs) without affecting outer hair cells (OHCs) or thresholds, because the synaptopathy occurs first in high-threshold ANFs. However, the fiber loss likely impairs temporal processing and hearing-in-noise, a classic complaint of those with sensorineural hearing loss. Non-human primates appear to be less vulnerable to noise-induced hair-cell loss than rodents, but their susceptibility to synaptopathy has not been studied. Because establishing a non-human primate model may be important in the development of diagnostics and therapeutics, we examined cochlear innervation and the damaging effects of acoustic overexposure in young adult rhesus macaques. Anesthetized animals were exposed bilaterally to narrow-band noise centered at 2 kHz at various sound-pressure levels for 4 hrs. Cochlear function was assayed for up to 8 weeks following exposure via auditory brainstem responses (ABRs) and otoacoustic emissions (OAEs). A moderate loss of synaptic connections (mean of 12-27% in the basal half of the cochlea) followed temporary threshold shifts (TTS), despite minimal hair-cell loss. A dramatic loss of synapses (mean of 50-75% in the basal half of the cochlea) was seen on IHCs surviving noise exposures that produced permanent threshold shifts (PTS) and widespread hair-cell loss. Higher noise levels were required to produce PTS in macaques compared to rodents, suggesting that primates are less vulnerable to hair-cell loss. However, the phenomenon of noise-induced cochlear synaptopathy in primates is similar to that seen in rodents.
There is now a good deal of data from neurophysiological studies in animals and behavioral studies in human infants regarding the development of multisensory processing capabilities. Although the conclusions drawn from these different datasets sometimes appear to conflict, many of the differences are due to the use of different terms to mean the same thing and, more problematic, the use of similar terms to mean different things. Semantic issues are pervasive in the field and complicate communication among groups using different methods to study similar issues. Achieving clarity of communication among different investigative groups is essential for each to make full use of the findings of others, and an important step in this direction is to identify areas of semantic confusion. In this way investigators can be encouraged to use terms whose meaning and underlying assumptions are unambiguous because they are commonly accepted. Although this issue is of obvious importance to the large and very rapidly growing number of researchers working on multisensory processes, it is perhaps even more important to the noncognoscenti. Those who wish to benefit from the scholarship in this field but are unfamiliar with the issues identified here are most likely to be confused by semantic inconsistencies. The current
(VOR). If the VOR undergoes adaptive modification with spectacles that change the magnification of the visual scene, signals in one neural pathway are modified, whereas those in another are not. By recording the responses of vestibular afferents and abducens neurons for vestibular oscillations at frequencies from 0.5 to 50 Hz, we have elucidated how vestibular signals are processed in the modified versus unmodified VOR pathways. For the small stimuli we used (Ϯ15°/s), the afferents with the most regular spontaneous discharge fired throughout the cycle of oscillation even at 50 Hz, whereas afferents with more irregular discharge showed phase locking. For all afferents, the firing rate was in phase with stimulus head velocity at low frequencies and showed progressive phase lead as frequency increased. Sensitivity to head velocity increased steadily as a function of frequency. Abducens neurons showed highly regular spontaneous discharge and very little evidence of phase locking. Their sensitivity to head velocity during the VOR was relatively flat across frequencies; firing rate lagged head velocity at low frequencies and shifted to large phase leads as stimulus frequency increased. When afferent responses were provided as inputs to a two-pathway model of the VOR, the output of the model reproduced the responses of abducens neurons if the unmodified and modified VOR pathways had frequency-dependent internal gains and included fixed time delays of 1.5 and 9 ms. The phase shifts predicted by the model provide fingerprints for identifying brain stem neurons that participate in the modified versus unmodified VOR pathways. I N T R O D U C T I O NThe rotatory vestibuloocular reflex (VOR) is an excellent system for understanding how neural circuits generate simple behaviors. VOR performance has been studied thoroughly and the neural circuit is localized in the brain stem and cerebellum, where it can be studied in awake animals. The inputs to the horizontal rotatory VOR arise from vestibular primary afferents of the horizontal semicircular canal, which discharge in relationship to head velocity and acceleration. At the outputs, motoneurons in the abducens nucleus discharge in relation to eye velocity and position. Afferents and motoneurons are connected by a series of parallel pathways, the shortest of which include only one interneuron.Most of what we know about the operation of the neural circuits for the VOR comes from recordings made during the VOR induced by either low-frequency sinusoidal head oscillation or brief pulses of head velocity. In general, these stimuli have statistics that fall within the range found in head turns ( (1973) showed that signal transformations for the VOR can be modeled as two parallel pathways: 1) a velocity pathway that transmits afferent signals with little modification to provide the eye velocity component of motoneuron firing and 2) a position pathway that integrates the vestibular inputs to provide the eye position component of motoneuron firing. Second, Lisberger (1984, 1994 provi...
The head-related transfer function (HRTF) of the cat adds directionally dependent energy minima to the amplitude spectrum of complex sounds. These spectral notches are a principal cue for the localization of sound source elevation. Physiological evidence suggests that the dorsal cochlear nucleus (DCN) plays a critical role in the brainstem processing of this directional feature. Type O units in the central nucleus of the inferior colliculus (ICC) are a primary target of ascending DCN projections and, therefore, may represent midbrain specializations for the auditory processing of spectral cues for sound localization. Behavioral studies confirm a loss of sound orientation accuracy when DCN projections to the inferior colliculus are surgically lesioned. This study used simple analogs of HRTF notches to characterize single-unit response patterns in the ICC of decerebrate cats that may contribute to the directional sensitivity of the brain's spectral processing pathways. Manipulations of notch frequency and bandwidth demonstrated frequency-specific excitatory responses that have the capacity to encode HRTF-based cues for sound source location. These response patterns were limited to type O units in the ICC and have not been observed for the projection neurons of the DCN. The unique spectral integration properties of type O units suggest that DCN influences are transformed into a more selective representation of sound source location by a local convergence of wideband excitatory and frequency-tuned inhibitory inputs.
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