Multisensory and unisensory neurons in ferret parietal cortex exhibit distinct functional properties.

Despite the fact that unisensory and multisensory neurons are comingled in every neural structure in which they have been identified, no systematic comparison of their response features has been conducted. Towards that goal, the present study was designed to examine and compare measures of response magnitude, latency, duration and spontaneous activity in unisensory and bimodal neurons from the ferret parietal cortex. Using multichannel single-unit recording, bimodal neurons were observed to demonstrate significantly higher response levels and spontaneous discharge rates than did their unisensory counterparts. These results suggest that, rather than merely reflect different connectional arrangements, unisensory and multisensory neurons are likely to differ at the cellular level. Thus, it can no longer be assumed that the different populations of bimodal and unisensory neurons within a neural region respond similarly to a given external stimulus.

Adult deafness induces somatosensory conversion of ferret auditory cortex.

In response to early or developmental lesions, responsiveness of sensory cortex can be converted from the deprived modality to that of the remaining sensory systems. However, little is known about capacity of the adult cortex for cross-modal reorganization. The present study examined the auditory cortices of animals deafened as adults, and observed an extensive somatosensory conversion within as little as 16 days after deafening. These results demonstrate that cortical cross-modal reorganization can occur after the period of sensory system maturation.

Neuroanatomical identification of crossmodal auditory inputs to interneurons in somatosensory cortex.

Multisensory convergence is the first, requisite step in the process that generates neural responses to events involving more than one sensory modality. Although anatomical studies have documented the merging of afferents from different sensory modalities within a given area, they do not provide insight into the architecture of connectivity at the neuronal level that underlies multisensory processing. In fact, few anatomical studies of multisensory convergence at the neuronal level have been conducted. The present study used a combination of tract-tracing, immunocytochemistry, and confocal microscopic techniques to examine the connections related to crossmodal auditory cortical inputs to somatosensory area SIV. Axons labeled from auditory cortex were found in contact with immunolabeled interneurons in SIV, some of which also colocalized vesicular glutamate transporter 1, indicating the presence of an active, glutamatergic synapse. No specific subtype of inhibitory interneuron appeared to be targeted by the crossmodal contacts. These results provide insight into the structural basis for multisensory processing at the neuronal level and offer anatomical evidence for the direct involvement of inhibitory interneurons in multisensory processing.

What is a multisensory cortex? A laminar, connectional, and functional study of a ferret temporal cortical multisensory area.

Now that examples of multisensory neurons have been observed across the neocortex, this has led to some confusion about the features that actually designate a region as "multisensory." While the documentation of multisensory effects within many different cortical areas is clear, often little information is available about their proportions or net functional effects. To assess the compositional and functional features that contribute to the multisensory nature of a region, the present investigation used multichannel neuronal recording and tract tracing methods to examine the ferret temporal region: the lateral rostral suprasylvian sulcal area. Here, auditory-tactile multisensory neurons were predominant and constituted the majority of neurons across all cortical layers whose responses dominated the net spiking activity of the area. These results were then compared with a literature review of cortical multisensory data and were found to closely resemble multisensory features of other, higher-order sensory areas. Collectively, these observations argue that multisensory processing presents itself in hierarchical and area-specific ways, from regions that exhibit few multisensory features to those whose composition and processes are dominated by multisensory activity. It seems logical that the former exhibit some multisensory features (among many others), while the latter are legitimately designated as "multisensory."

Not just for bimodal neurons anymore: the contribution of unimodal neurons to cortical multisensory processing.

Traditionally, neuronal studies of multisensory processing proceeded by first identifying neurons that were overtly multisensory (e.g., bimodal, trimodal) and then testing them. In contrast, the present study examined, without precondition, neurons in an extrastriate visual area of the cat for their responses to separate (visual, auditory) and combined-modality (visual and auditory) stimulation. As expected, traditional bimodal forms of multisensory neurons were identified. In addition, however, many neurons that were activated only by visual stimulation (i.e., unimodal) had that response modulated by the presence of an auditory stimulus. Some unimodal neurons showed multisensory responses that were statistically different from their visual response. Other unimodal neurons had subtle multisensory effects that were detectable only at the population level. Most surprisingly, these non-bimodal neurons generated more than twice the multisensory signal in the PLLS than did the bimodal neurons. These results expand the range of multisensory convergence patterns beyond that of the bimodal neuron. However, rather than characterize a separate class of multisensory neurons, unimodal multisensory neurons may actually represent an intermediary form of multisensory convergence that exists along the functional continuum between unisensory neurons, at one end, and fully bimodal neurons at the other.

Do cross-modal projections always result in multisensory integration?

Convergence of afferents from different sensory modalities has generally been thought to produce bimodal (and trimodal) neurons (i.e., exhibit suprathreshold excitation to more than 1 sensory modality). Consequently, studies identifying cross-modal connections assume that such convergence results in bimodal (or trimodal) neurons that produce familiar forms of multisensory integration: response enhancement or depression. The present study questioned that assumption by anatomically identifying a projection from ferret auditory to visual cortex Area 21. However, electrophysiological recording within Area 21 not only failed to identify a single bimodal neuron but also familiar forms of multisensory integration were not observed either. Instead, a small proportion of neurons (9%; 27/296) showed subthreshold multisensory integration, in which visual responses were significantly modulated by auditory inputs. Such subthreshold multisensory effects were enhanced by gamma-aminobutyric acid antagonism, whereby a majority of neurons (87%; 20/23) now participated in a significant, multisensory population effect. Thus, multisensory convergence does not de facto result in bimodal (or trimodal) neurons or the traditional forms of multisensory integration. However, the fact that unimodal neurons exhibited a subthreshold form of multisensory integration not only affirms the relationship between convergence and integration but also expands our understanding of the functional repertoire of multisensory processing itself.

Modeling of multisensory convergence with a network of spiking neurons: a reverse engineering approach.

Multisensory processing in the brain underlies a wide variety of perceptual phenomena, but little is known about the underlying mechanisms of how multisensory neurons are formed. This lack of knowledge is due to the difficulty for biological experiments to manipulate and test the parameters of multisensory convergence, the first and definitive step in the multisensory process. Therefore, by using a computational model of multisensory convergence, this study seeks to provide insight into the mechanisms of multisensory convergence. To reverse-engineer multisensory convergence, we used a biologically realistic neuron model and a biology-inspired plasticity rule, but did not make any a priori assumptions about multisensory properties of neurons in the network. The network consisted of two separate projection areas that converged upon neurons in a third area, and stimulation involved activation of one of the projection areas (or the other) or their combination. Experiments consisted of two parts: network training and multisensory simulation. Analyses were performed, first, to find multisensory properties in the simulated networks; second, to reveal properties of the network using graph theoretical approach; and third, to generate hypothesis related to the multisensory convergence. The results showed that the generation of multisensory neurons related to the topological properties of the network, in particular, the strengths of connections after training, was found to play an important role in forming and thus distinguishing multisensory neuron types.

Auditory influences on non-auditory cortices.

Although responses to auditory stimuli have been extensively examined in the well-known regions of auditory cortex, there are numerous reports of acoustic sensitivity in cortical areas that are dominated by other sensory modalities. Whether in 'polysensory' cortex or in visual or somatosensory regions, auditory responses in non-auditory cortex have been described largely in terms of auditory processing. This review takes a different perspective that auditory responses in non-auditory cortex, either through multisensory subthreshold or bimodal processing, provide subtle but consistent expansion of the range of activity of the dominant modality within a given area. Thus, the features of these acoustic responses may have more to do with the subtle adjustment of response gain within a given non-auditory region than the encoding of their tonal properties.

Subthreshold auditory inputs to extrastriate visual neurons are responsive to parametric changes in stimulus quality: sensory-specific versus non-specific coding.

A new subthreshold form of multisensory processing has been recently identified that results from the convergence of suprathreshold excitatory inputs from one modality with subthreshold inputs from another. Because of the subthreshold nature of the second modality, descriptive measures of sensory features such as receptive field properties or location are not directly apparent as they are for traditional bimodal neurons. This raises the question of whether or not subthreshold signals actually convey sensory-specific receptive field information as seen in their bimodal counterparts, or if they represent non-specific effects such as arousal. The present experiment addressed this issue in visually-responsive neurons from the cat posterolateral lateral suprasylvian cortex (PLLS). Single-unit electrophysiological techniques were used to record neuronal responses to visual, auditory and combined visual-auditory stimuli while the intensity of stimulation in the subthreshold auditory modality was systematically altered. The results showed that subthreshold multisensory neurons were sensitive to changes in auditory stimulus intensity. These receptive field sensitivities are similar to those observed in bimodal neurons and thereby represent sensory-specific, not arousal-related responses. In addition, these results provide further support for the notion that multisensory processing occurs along a dynamic continuum of neuronal convergence patterns from bimodal to purely sensory-specific.

Cross-modal circuitry between auditory and somatosensory areas of the cat anterior ectosylvian sulcal cortex: a 'new' inhibitory form of multisensory convergence.

Examples of convergence of visual and auditory, or visual and somatosensory, inputs onto individual neurons abound throughout the brain, but substantially fewer incidences of auditory-somatosensory neurons have been reported. The present experiments sought to examine auditory-somatosensory convergence to assess whether there is a feature of this type of convergence that might obscure it from conventional methods of multisensory detection. Auditory-somatosensory convergence was explored in cat anterior ectosylvian sulcus (AES) cortex, where higher-order somatosensory area IV (SIV) and auditory field of the anterior ectosylvian sulcus (FAES) share a common border. While neuroanatomical tracers documented a projection from FAES to SIV, physiological studies failed to reveal the bimodal neurons expected from such cross-modal connectivity. Stimulation of FAES through indwelling electrodes also failed to excite any of the SIV neurons examined. However, when stimulation of auditory FAES was combined with somatosensory stimulation, a large majority (66%) of SIV neurons showed a significant response attenuation. FAES-induced response suppression was specific to SIV, could not be elicited by activating other auditory regions and was blocked by the microiontophoretic application of the GABAergic antagonist bicuculline methiodide. Based on these data, a novel, cross-modal circuit is proposed involving projections from auditory FAES to somatosensory SIV, where local inhibitory interneurons 'reverse the sign' of the cross-modal signals to produce auditory-somatosensory suppression. This form of excitatory-inhibitory multisensory convergence has not been reported before and suggests that the level of interaction between auditory and somatosensory modalities has been substantially underestimated.