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.

Hypotheses Relating to the Function of the Claustrum

“…In our previous hypothesis (Smythies et al, 2012) it was thought that to do this the claustrum needed direct inputs to individual claustral cells from axons derived from the two disparate cortices. The data recently obtained by Remedios et al (2010) suggest that these direct connections do not exist. However, in our present model, such direct connections are not necessary, because the majority of the "binding" is done inside the claustrum.…”

“…The first is that the gamma signal may not just convey the signal "match," but it may also carry information about what has been matched, in which case a null signal would not be sufficient. Secondly, in the Remedios et al (2010) experiment, the stimulus was a "familiar jungle scene." Therefore, the animal was expecting it, and the signal recorded by the experiments might have been a "match" signal.…”

“…They conclude that this shows that the claustrum, in rats, does not function as an integrator of somesthetic and motor function. The experiments of Remedios et al (2010), however, show that there is a rapid functional connection between the auditory system and the claustrum. Moreover, Zhang et al (2001), using a similar technique, were able to demonstrate bidirectional connections between the claustrum, on the one hand, and both primary and secondary visual, somatosensory, and auditory cortices on the other.…”

“…The injection of three different fluorescent tracers into the occipital, frontal, and cingulate cortices results in double-and triple-labeled cells in the claustrum (Li et al, 1986). In contrast, a recent investigation in awake primates found that the great majority of claustral neurons are unimodal (Remedios et al, 2010). On the efferent side, using similar techniques Minciacchi et al (1985) reported that single claustral neurons project to both anterior and posterior cortex, some ipsilaterally and some contralaterally.…”

The claustrum: Considerations regarding its anatomy, functions and a programme for research

“…As we have alluded to already, and perhaps understandably given the elaborate claustral connectome, the possible functions of the claustrum have received considerable attention, with many hypotheses posed (Goll et al, 2015;Mathur, 2014;Remedios et al, 2010Remedios et al, , 2014Smythies et al, 2012b). Most recently, two related articles (Smythies et al, 2012a;Yin et al, 2016) suggest that complex connectivity and organisation of the claustrum is Like cortico-thalamic inputs, cortico-claustral inputs are predominantly derived from cortical layer 6, while claustro-cortical inputs are predominantly to cortical layer 4, suggesting that they may comprise a driver input rather than a modulatory one.…”