Unimodal responses prevail within the multisensory claustrum

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. Copyright © 2010 the authors.

Annotations for: Unimodal responses prevail within the multisensory claustrum

Background

While the exact function of the claustrum remains speculative, recent studies have assigned an integrative role to it. [@remediosUnimodalResponsesPrevail2010, p. 12902]

Hypothesis

In this study we directly tested the hypothesis that claustral neurons participate in integrating stimuli across the sensory modalities. [@remediosUnimodalResponsesPrevail2010, p. 12902]

recorded neural responses in the claustrum of alert nonhuman primates to audio-visual stimuli [@remediosUnimodalResponsesPrevail2010, p. 12902]

Methods

Two adult male rhesus monkeys [@remediosUnimodalResponsesPrevail2010, p. 12902]

Neural activity was recorded in response to an audio-visual stimulation paradigm while the animals performed a visual fixation task [@remediosUnimodalResponsesPrevail2010, p. 12903]

Naturalistic 1 s long auditory (sound only), visual (video only) and bimodal audio-visual stimuli (sound&video) were presented [@remediosUnimodalResponsesPrevail2010, p. 12903]

stimuli comprised videos and sounds of behaviorally relevant scenes, such as movies of vocalizing conspecifics or other animals in their natural settings [@remediosUnimodalResponsesPrevail2010, p. 12903]

The “response amplitude” for each unit and modality condition was computed by first finding the peak of the trial averaged response and then computing (for each trial) the mean spike count in a 100 ms time window centered on this peak. [@remediosUnimodalResponsesPrevail2010, p. 12903]

Wilcoxon rank-sum test, and units with a significant ( p 0.05) difference were labeled by the modality eliciting the stronger response. [@remediosUnimodalResponsesPrevail2010, p. 12903]

“Bimodal” neurons were defined as neurons responding with (significant) deviations from baseline to both visual and acoustic stimuli [@remediosUnimodalResponsesPrevail2010, p. 12903]

Results

claustral responses to the same sounds were stereotyped and consisted of a strong transient followed by a minimal sustained response [@remediosUnimodalResponsesPrevail2010, p. 12904]

Of the neurons assigned to the claustrum, some responded during the presentation of the video but not during the presentation of the sound, while some responded to the sound but not the video [@remediosUnimodalResponsesPrevail2010, p. 12904]

One striking result emerging from our data is that these groups of neurons with visual and acoustic preferences were spatially separated. [@remediosUnimodalResponsesPrevail2010, p. 12904]

results corroborate earlier reports of discrete sensory zones within the claustrum that are connected to the corresponding primary sensory cortical areas (Olson and Graybiel, 1980) [@remediosUnimodalResponsesPrevail2010, p. 12904]

neurons responding to the sound but not the video (upper examples) were encountered 20 mm from the cortical surface, while neurons responding to the video but not the sound (lower examples) were encountered a further 6 mm deeper. [@remediosUnimodalResponsesPrevail2010, p. 12904]

auditory zone generally responded to sounds with a transient response followed by a smaller sustained response during the 1 s stimulus period [@remediosUnimodalResponsesPrevail2010, p. 12904]

visual zone responded to visual stimuli with a prominent onset response followed by a sustained elevation of firing during the rest of the video [@remediosUnimodalResponsesPrevail2010, p. 12904]

Across both claustral zones we found that the two populations of neurons respond preferentially to their preferred modality and respond only minimally to stimuli in the other modality [@remediosUnimodalResponsesPrevail2010, p. 12905]

Consistently across both claustral zones we did not find response interactions between nonspecific stimuli presented to a particular modality. [@remediosUnimodalResponsesPrevail2010, p. 12905]

Conclusions

Our results show that while the claustrum, as a structure, responds to stimuli in different sensory modalities, individual neurons show little evidence for multisensory processing. [@remediosUnimodalResponsesPrevail2010, p. 12905]

Our results suggest that the claustrum is not a simple relay for sensory information between cortical structures. For example, responses of neurons in the auditory zone to long naturalistic sounds consisted only of a brief transient following sound onset and did not reflect the full structure or duration of the sound (cf. Fig. 2). [@remediosUnimodalResponsesPrevail2010, p. 12906]

Implications

Our results underscore the need for rethinking the function of the claustrum, [@remediosUnimodalResponsesPrevail2010, p. 12906]

While our results demonstrate that the claustrum as structure has access to different sensory modalities, our results challenge the notion that it integrates information across these modalities. [@remediosUnimodalResponsesPrevail2010, p. 12906]

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