Visual- and saccade-related signals in the primate inferior colliculus

Center for Cognitive Neuroscience, Department of Psychology and Neuroscience and Department of Neurobiology, Duke University, Durham, NC 27708

Edited by Eric I. Knudsen, Stanford University School of Medicine, Stanford, CA, and approved August 23, 2007 (received for review July 3, 2007)

Abstract

The inferior colliculus (IC) is normally thought of as a predominantly auditory structure because of its early position in the ascending auditory pathway just before the auditory thalamus. Here, we show that a majority of IC neurons (64% of 180 neurons) in awake monkeys carry visual- and/or saccade-related signals in addition to their auditory responses (P < 0.05). The response patterns involve primarily excitatory visual responses, but also increased activity time-locked to the saccade, slow rises in activity time-locked to the onset of the visual stimulus, and inhibitory responses. The presence of these visual-related signals suggests that the IC plays a role in integrating visual and auditory information. More broadly, our results show that interactions between sensory pathways can occur at very early points in sensory processing streams, which implies that multisensory integration may be a low-level rather than an exclusively high-level process.

Footnotes

^†To whom correspondence should be addressed. E-mail: jmgroh{at}duke.edu
Author contributions: K.K.P. designed research; K.K.P. and R.R.M. performed research; K.K.P. and J.M.G. analyzed data; and J.M.G. wrote the paper with input from K.K.P. and R.R.M.
↵*Present address: School of Medicine, University of Alabama at Birmingham, Birmingham, AL 35294.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
↵ ‡ A preliminary version of this work has been presented [ref. 46 and Porter, K. K., Metzger, R. R., Werner-Reiss, U., Underhill, A. M., Groh, J. M. (2005) Soc Neurosci Abstr, program no 505.4].
This article contains supporting information online at www.pnas.org/cgi/content/full/0706249104/DC1.
↵ § The probability that this proportion of neurons would appear by chance if the IC does not truly contain visually responsive neurons is <1 × 10⁻¹⁴ (one-tailed binomial test).
↵ ¶ For both of the neurons shown in Fig. 4 a and b, the vigor of the discharge was slightly greater on trials involving longer saccade reaction times (trials shown at the bottom of the raster plot). Whether this is truly related to the saccade reaction time or some other covarying factor such as motivation is an issue that can be addressed in future experiments in which reaction time is controlled, such as with a delayed saccade paradigm.
↵ ‖ Metzger, R. R., Kelly, K. A., Groh, J. M. (2004) Soc Neurosci Abstr30:177.21.
Abbreviations:

IC,

inferior colliculus;

SC,

superior colliculus;

PETH,

perievent time histogram;

LED,

light-emitting diode.
Freely available online through the PNAS open access option.