Unimodal responses prevail within the multisensory claustrum

Abstract

The claustrum receives afferent inputs from multiple sensory-related brain areas, prompting speculation about a role in integrating information across sensory modalities. Here we directly test this hypothesis by probing neurons in the primate claustrum for functional characteristics of multisensory processing. To this end we recorded neuronal responses to naturalistic audio-visual stimuli from the claustra of alert monkeys. Our results reveal the existence of distinct claustral zones comprised of unimodal neurons associated with the auditory and visual modalities. In a visual zone within the ventral claustrum neurons responded to visual stimuli but not to sounds, whereas in an auditory zone located within the central claustrum neurons responded to sounds but not to visual stimuli. Importantly, we find that neurons within either zone are not influenced by stimuli in the other modality and do not exhibit the typical response characteristics usually associated with multisensory processing. While these results confirm the notion of the claustrum as a multisensory structure per se, they argue against the hypothesis of the claustrum serving as an integrator of sensory information.

Figure 1.

Auditory and visual zones in the claustrum. A, Illustration of the vertical approach to the claustrum used in one animal, depicted on an anatomical MR image. B, Timeline of the audio-visual stimulation paradigm. C, Nissl-stained section used to confirm the approach to the claustrum using visible electrode tracks. Approximate locations of the auditory and visual zones are indicated. D, Example data recorded on three penetrations demonstrating the subsequent occurrence of auditory and visually driven units at different depths from the cortical surface. Lines denote the trial-averaged firing rate to visual (video), auditory (sound) and combined audio-visual (sound&video) stimuli (smoothed using a 10 ms Gaussian window); baseline firing rates were subtracted. Stimuli commenced at t = 0. cla, claustrum; ins, insular cortex; ac, auditory cortex; ls, lateral sulcus.

Figure 2.

Unimodal responses in the auditory and visual zones. A, Schematic of the claustrum with auditory (green) and visual (red) zones. B, Population response within each zone to visual, auditory and combined audio-visual stimuli (median across neurons; auditory zone n = 148; visual zone n = 43). Neurons within the auditory zone responded to sounds and video and sound pairs, but not to the video alone. Neurons within the visual zone responded to videos but not to sounds. C, Responses of all units to each modality condition. Response amplitudes are color coded (red, high response) and have been normalized across neurons for display purposes. D, Distribution of response amplitudes across units (boxplots indicate the median and 25^th and 75^th percentiles).

Figure 3.

Modality preferences and lack of multisensory response interactions. A, Modality preferences established by comparing responses to sounds and videos. B, Response amplitudes to sounds and videos for individual units (dots). Units are color-coded according to their modality preference. Units depicted as circles were flagged as statistically significant bimodal, i.e., as exhibiting significant responses to both sensory modalities. C, Response amplitudes to audio-visual stimuli compared with the linear superposition of the responses to unimodal auditory and visual stimuli. A statistical bootstrap test revealed that only a negligible fraction of units (circles) exhibits statistically significant deviations from a linear superposition.