Multisensory Enhancement in the Optic Tectum of the Barn Owl: Spike Count and Spike Timing

Abstract

Zahar Y, Reches A, Gutfreund Y. Multisensory enhancement in the optic tectum of the barn owl: spike count and spike timing. J Neurophysiol 101: 2380 -2394, 2009. First published March 4, 2009 doi:10.1152/jn.91193.2008. Temporal and spatial correlations between auditory and visual stimuli facilitate the perception of unitary events and improve behavioral responses. However, it is not clear how combined visual and auditory information is processed in single neurons. Here we studied responses of multisensory neurons in the barn owl's optic tectum (the avian homologue of the superior colliculus) to visual, auditory, and bimodal stimuli. We specifically focused on responses to sequences of repeated stimuli. We first report that bimodal stimulation tends to elicit more spikes than in the responses to its unimodal components (a phenomenon known as multisensory enhancement). However, this tendency was found to be historydependent; multisensory enhancement was mostly apparent in the first stimulus of the sequence and to a much lesser extent in the subsequent stimuli. Next, a vector-strength analysis was applied to quantify the phase locking of the responses to the stimuli. We report that in a substantial number of multisensory neurons responses to sequences of bimodal stimuli elicited spike trains that were better phase locked to the stimulus than spike trains elicited by stimulating with the unimodal counterparts (visual or auditory). We conclude that multisensory enhancement can be manifested in better phase locking to the stimulus as well as in more spikes.

Interactions between Stimulus-Specific Adaptation and Visual Auditory Integration in the Forebrain of the Barn Owl

“…Congruent bimodal stimuli are likely to arise from the same object and therefore provide complementary information, whereas incongruent bimodal stimuli are not and thus provide competing information. Consistent with this is the common observation that the presentation of congruent audiovisual stimulation leads to enhancement over the unimodal responses, whereas incongruent stimuli lead to no enhancement or even suppression compared with the unimodal responses (King and Palmer, 1985;Meredith and Stein, 1986a;Wallace et al, 1992;Reches and Gutfreund, 2009;Zahar et al, 2009). If the multisensory integration reported here plays a role in increasing the probability of detecting deviant objects, we expect the enhancement to appear when the information is likely to be complementary and to be absent when the information is not complementary.…”

“…Recently, we have reported in tectal neurons that, in a monotonic sequence of sensory events, the first, less expected event usually gives rise to stronger multisensory enhancement compared with the subsequent events (Zahar et al, 2009). In addition, Bergan and Knudsen (2009) have reported enhanced modulation of auditory responses in the inferior colliculus of barn owls by rare visual stimuli (presumably via visual signals from the OT).…”

“…Both basic phenomena, unisensory SSA and enhancement of responses to congruent bimodal stimuli, have been reported in tectal neurons of the barn owl (Reches and Gutfreund, 2008;Zahar et al, 2009). Therefore, on the basis of the available physiological data, it is difficult to distinguish between the two models (described above and in Fig.…”

Stimulus-specific adaptation, habituation and change detection in the gaze control system

“…Thus, neural responses in the tectum seem unable to code unambiguously the sensory identity of the incoming sound. This, together with the finding that OT/SC neurons are mostly broadly tuned to sensory features, such as frequency, amplitude modulations, orientation, direction, and modality, (Mize and Murphy 1976;Zahar et al 2009) is consistent with the hypothesis that indicating the exact identity of the stimulus is not a computational task of the OT. The OT represents the location of the stimulus and how salient it is in time and space.…”

“…2), as well as indirectly from visual forebrain areas (Karten et al 1973), giving rise to a retinotopic representation of visual space (Knudsen 1982). Since the superficial and deep layers are functionally connected, many neurons in the OT are multisensory, responding to both visual and auditory signals inside their receptive fields (Brainard and Knudsen 1998;Zahar et al 2009). …”