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Hypotheses Relating to the Function of the Claustrum

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Hypotheses Relating to the Function of the Claustrum HYPOTHESIS AND THEORY ARTICLE published: 02 August 2012 INTEGRATIVE NEUROSCIENCE doi: 10.3389/fnint.2012.00053 Hypotheses relating to the function of the claustrum John Smythies1*, Lawrence Edelstein 2 and Vilayanur Ramachandran1 1 Center for Brain and Cognition, University of California San Diego, La Jolla, CA, USA 2 Medimark Corporation, Del Mar, CA, USA Edited by: This paper presents a new hypothesis as to the function of the claustrum. Our basic Warren H. Meck, Duke University, premise is that the claustrum functions as a detector and integrator of synchrony in the USA axonal trains in its afferent inputs. In the first place an unexpected stimulus sets up a Reviewed by: processed signal to the sensory cortex that initiates a focus of synchronized gamma Warren H. Meck, Duke University, USA oscillations therein. This focus may then interact with a general alerting signal conveyed Antonio Pereira, Federal University from the reticular formation via cholinergic mechanisms, and with other salient activations of Rio Grande do Norte, Brazil set up by the stimulus in other sensory pathways that are relayed to the cortex. This *Correspondence: activity is relayed from the cortex to the claustrum, which then processes these several John Smythies, Center for Brain and inputs by means of multiple competitive intraclaustral synchronized oscillations at different Cognition, University of California San Diego, 9500 Gilman Drive, frequencies. Finally it modulates the synchronized outputs that the claustrum distributes La Jolla, CA 92039, USA. to most cortical and many subcortical structures, including the motor cortex. In this e-mail: jsmythies@ucsd.edu way, during multicenter perceptual and cognitive operations, reverberating claustro-cortical loops potentiate weak intracortical synchronizations by means of connected strong intraclaustral synchronizations. These may also occur without a salient stimulus. By this mechanism, the claustrum may play a strong role in the control of interactive processes in different parts of the brain, and in the control of voluntary behavior. These may include the neural correlates of consciousness. We also consider the role of GABAergic mechanisms and deafferentation plasticity. Keywords: claustrum, binding, GABAergic interneurons, salience, consciousness, synchrony, oscillations INTRODUCTION published evidence, based on experiments that employed injec- In 2005 Crick and Koch suggested that the claustrum might play tions of cholera toxin B (CTB), and biotinylated dextran amine a key role in information processing in the brain by correlat- tracers, application of antibodies to GABA and glutamic acid ing the separate activity in the different sensory cortices into one decarboxylase, and confocal and electron microscopy, that the coherent activity that “binds” separate sensations into the unitary two have reciprocal connections. They also noted that four times objects that we experience in consciousness. In a previous paper as many cells were labeled in the claustrum as compared to the (Smythies et al., 2012)weoutlinedanhypothesisastohowthis dorsal lateral geniculate nucleus following V1 CTB injections. “binding” process might be effected. This hypothesis, however, The auditory cortex may have somewhat different claustral proved to be unsatisfactory. The present paper presents a new connections than the visual and somatosensory cortices. Clarey hypothesis that includes not only an account of sensory binding and Irvine (1986) report than, in the cat, the input from the pri- but a number of other functions of the claustrum as well. mary auditory area to the claustrum is sparse and comes rather The claustrum is broadly divided into three compartments from higher auditory areas. Beneyto and Prieto (2001)studied [an anterior-dorsal connected with the somatosensory and motor the connections between the claustrum and the auditory cortex cortices, a posterior dorsal (visual cortex) and a ventral area by tracer injection methods. They report that all auditory areas (auditory cortex)] (LeVay and Sherk, 1981; Sherk and LeVay, have reciprocal connections with the ipsi- and contralateral claus- 1981; Sherk, 1986; Edelstein and Denaro, 2004; Crick and Koch, trum. They state, “These findings suggest that the intermediate 2005). The claustrum has reciprocal widely distributed anatom- region of the claustrum integrates inputs from all auditory cor- ical projections to almost all regions of the cortex, as well as tical areas, and then sends the result of such processing back to many subcortical structures. A recent high definition diffu- to every auditory cortical field.” By means of differential bidi- sion imaging study (Park et al., 2012) reports that the claustrum rectional tracer injection experiments in mouse somatosensory has connections with the frontal, premotor, ventral anterior cin- cortex Smith et al. (2012) failed to find any significant anatom- gulate, ventral temporal, visual, motor, somatosensory, olfactory ical projections from the primary somatosensory cortex S1 to cortices, and most strongly with the entorhinal cortex. It also the claustrum, whereas they detected dense projections from the has connections with some subcortical structures including the same part of the claustrum to both S1 and the motor cortex. putamen, globus pallidus, and lateral amygdala. Until recently, They conclude that this shows that the claustrum, in rats, does however, the connections between the claustrum and V1 were the not function as an integrator of somesthetic and motor func- subject of some disagreement. Day-Brown et al. (2009)havenow tion. The experiments of Remedios et al. (2010), however, show Frontiers in Integrative Neuroscience www.frontiersin.org August 2012 | Volume 6 | Article 53 | 1 Smythies et al. Hypotheses relating to the function of the claustrum that there is a rapid functional connection between the auditory (Churchland and Sejnowski, 1999), or non-linear dynamics system and the claustrum. Moreover, Zhang et al. (2001), using a (Freeman, 2011), or synchronized oscillations (Uhlhaas et al., similar technique, were able to demonstrate bidirectional connec- 2009). In this paper we will focus on the last. One task the tions between the claustrum, on the one hand, and both primary claustrum performs may be to provide the cortex with infor- and secondary visual, somatosensory, and auditory cortices on mation that allows the cortex to “bind” certain of its on-going the other. activities. In addition the claustrum may not involved solely in The claustrum has a well-marked retinotopically organized sensory “binding”, but it may also be concerned with synchrony map of the visual field, as well as an equivalent map of the detection and modulation in connection with salience processing somatosensory field (Olson and Graybiel, 1980; LeVay and Sherk, and a wide range of cognitive processes. 1981; Sherk and LeVay, 1981; Sherk, 1986). It has been claimed that areas of the claustrum in the cat sends “precisely recipro- OUR HYPOTHESIS cal” projections back to those area(s) of the cortex whence its Our basic hypothesis is that the claustrum functions as a syn- inputs derived (LeVay and Sherk, 1981; Sherk and LeVay, 1981; chrony detector, and modulator and integrator of synchronized Sherk, 1986). It has also been claimed that the projections to and oscillations (for background see König et al., 1996; Uhlhaas et al., from the claustrum are diffuse, but quite specific, in both direc- 2009). By “synchrony detector” we mean nothing more elabo- tions (one point to specific points) (Divac et al., 1978; Divac, rate than is implied in the application of two well established 1979; Sloniewski et al., 1986). Single cells in the claustrum have principles (1) that neurons respond more robustly to synchro- been reported to send branched axons to several cortical areas. nized bursts then to random spikes, and (2) that neurons tend to Thesamecellsreceiveinputfromtheseareas(Rahman and reproduce in their efferent outputs the pattern of synchronization Baizer, 2007). However, there are marked species differences in contained in their afferent inputs. No elaborate timing devices, the anatomy of the claustrum and others claim that the cortico- such as those found in the aural mechanisms used to compute claustral projection is more diffuse. Crick and Koch summarize the location of auditory stimuli (Jeffress, 1948; Grothe, 2003), are their view of the situation thus, “Most regions of the cortex implied. send a projection to the claustrum, usually to many parts of it. When an incoming sensory volley reaches the brain, there Thus, their mappings are far from being a precise local mapping are two immediate tasks the brain must perform. The first and tend to be somewhat global (that is, all to all, though not (1) is to determine whether the information contained in the completely so).” volley matches the brain’s expectation of what that informa- The ventral claustrum is also connected to limbic structures, tion should be. The second (2) is to find out if the stimu- such as the amygdala, subiculum, and cingulate cortex. The claus- lus signals a state of affairs that is potentially threatening or trum also has a relatively uniform microanatomical structure that rewarding. The mechanism for (1) entails that, early in the would allow what Crick and Koch describe as “widespread intra- afferent inflow, the incoming down-up messages are matched claustral interactions.” These, they suggest, may be in the form against the up-down messages of what the brain expects the of
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