REPRESENTATION AND INTEGRATION OF MULTIPLE SENSORY INPUTS IN PRIMATE
Wallace, M. T., L. K. Wilkinson and B. E. Stein.
Department of Neurobiology and Anatomy, Bowman Gray School of Medicine/Wake
Forest University, Winston-Salem, NC 27157.
APStracts 3:0069N, 1996.
SUMMARY AND CONCLUSIONS
1. The properties of visual-, auditory-, and somatosensory-responsive neurons,
as well as of neurons responsive to multiple sensory cues (i.e., multisensory)
were examined in the superior colliculus of the rhesus monkey. Although
superficial layer neurons responded exclusively to visual stimuli, and visual
inputs predominated in deeper layers, there was also a rich nonvisual and
multisensory representation in the superior colliculus. Over a quarter (27.8%)
of the deep layer population responded to stimuli from more than a single
sensory modality. In contrast, 37% responded only to visual cues, 17.6% to
auditory cues and 17.6% to somatosensory cues. Unimodal- and multisensory-
responsive neurons were clustered by modality. Each of these modalities was
represented in map-like fashion, and the different representations were in
alignment with one another. 2. Most deep layer visually-responsive neurons
were binocular and exhibited poor selectivity for such stimulus
characteristics as orientation, velocity and direction of movement. Similarly,
most auditory-responsive neurons had contralateral receptive fields, were
binaural, but had little frequency selectivity and preferred complex, broad-
band sounds. Somatosensory-responsive neurons were overwhelmingly
contralateral, high velocity, and rapidly adapting. Only rarely did
somatosensory-responsive neurons require distortion of subcutaneous tissue for
activation. 3. The spatial congruence among the different receptive fields of
multisensory neurons was a critical feature underlying their ability to
synthesize cross-modal information. 4. Combinations of stimuli could have very
different consequences in the same neuron, depending on their temporal and
spatial relationships. Generally, multisensory interactions were evident when
pairs of stimuli were separated from one another by less than 500 ms, and the
products of these interactions far exceeded the sum of their unimodal
components. Whether the combination of stimuli produced response enhancement,
response depression, or no interaction depended on the location of the stimuli
relative to one another and to their respective receptive fields. Maximal
response enhancements were observed when stimuli originated from similar
locations in space (as when derived from the same event) because they fell
within the excitatory receptive fields of the same multisensory neurons. If,
however, the stimuli were spatially disparate such that one fell beyond the
excitatory borders of its receptive field, either no interaction was produced
or this stimulus depressed the effectiveness of the other. Furthermore,
maximal response interactions were seen with the pairing of weakly effective
unimodal stimuli. As the individual unimodal stimuli became increasingly
effective, the levels of response enhancement to stimulus combinations
declined, a principle referred to as inverse effectiveness. Many of the
integrative principles seen here in the primate superior colliculus are
strikingly similar to those observed in the cat. These observations indicate
that a set of common principles of multisensory integration is adaptable in
widely divergent species living in very different ecological situations. 5.
Surprisingly, a few multisensory neurons had individual receptive fields that
were not in register with one another. This has not been noted in multisensory
neurons of other species, and these "anomalous" receptive fields could present
a daunting problem: stimuli originating from the same general location in
space cannot simultaneously fall within their respective receptive fields, a
stimulus pairing which may result in response depression. Conversely, stimuli
that originate from separate events and disparate locations (and fall within
their receptive fields) may result in response enhancement. However, the
spatial principle of multisensory integration did not apply in these cases.
Stimuli presented within their spatially disparate excitatory receptive fields
inhibited one another's effectiveness, and spatially coincident stimuli failed
to produce an interaction. 6. These observations underscore the critical
nature of developing aligned maps in order to ensure normal multisensory
integration and of developing neural and behavioral strategies to maintain map
alignment during overt behaviors.
Received 15 September 1995; accepted in final form 15 March 1996.
APS Manuscript Number J619-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1996 The American Physiological Society.
Published in APStracts on 16 April 96