A recent paper by Jankowski and O'Mara (2015) throws new light on the function of
the claustrum. These authors took recordings from 874 claustral neurons in unanesthetized
behaving rats that showed responses probably anchored to visual stimuli. These fell
into three categories—“place” neurons (38) that responded to the location of the rat,
“boundary” neurons (23) that responded to boundaries closing the rat's environment,
and “object” neurons (48) that fired only in response to the existence of a specific
object in the environment. All three types of response showed with good within-session
stability. Of particular interest in the present context are the object cells. These
code the position in space of an object in the environment and not its particular
properties (e.g., shape, texture, color). They also follow an object when it moves
in the environment. Some object neurons can follow multiple objects (up to 3). Object
neurons are also found in the subiculum, and in the anterior entorhinal, perirhinal,
and anterior cingulate cortices with which areas the claustrum has extensive connections.
The authors suggest that this system processes dynamic information about spatial features
of the environment relating to the location in space of the organism, and the presence
of important features in the environment such as boundaries and objects. The claustrum
then supplies this information to the wider brain systems in the hippocampus and related
cortices so as to facilitate the moment-to-moment control of behavior.
The question this opinion piece addresses is how does this new data relate to a current
hypothesis as to the function of the claustrum first put forward by Crick and Koch
(2005) and elaborated by Smythies et al. (2012, 2014)? This hypothesis suggests that
the claustrum integrates the sensorimotor mechanisms that control behavior via competitive
“winner-takes-all” synchronized gamma oscillations in the cortico-claustral circuits
by the Pearson system. This system states that, if two cortical areas A and B connect
by synchronized oscillations, and, if A connects to claustral area C and B connects
to claustral area D, then C, and D will be connected by synchronized oscillations.
However, if A and B are not so connected, then C and D will not be connected either.
One “low level” feature of our original hypothesis is that the “binding” of disparate
color, shape and movement sensations in the perception of a unitary perceptual object
may mediated by this synchronization of gamma oscillations. Another “high level” feature
of this hypothesis, also using competitive synchronized oscillations, is that circuits
linking the claustrum with higher cortex mediate voluntary decisions involving the
selection of particular behaviors in response to complex sensory and multisensory
inputs.
Four recent papers are relevant to this hypothesis.
Firstly, from experiments with brain slices, Orman (2015) has reported that the claustrum
has an intrinsic excitatory connectivity, manifesting as spontaneous synchronized
burst discharges, that is constrained in approximately rostro-caudal laminae, with
minimal cross-communication between laminae. This is compatible with our hypothesis.
The mainly rostro-caudal laminae provided by the Pearson mechanism do not interconnect
i.e., one active group ABCD does not interact with another active group EFGH.
Secondly, on the basis of a series of psychophysical experiments, that paired the
perception of color with motion or color with orientation, Zeki (2015) has proposed
that the brain is a massively asynchronous organ and has no central (master) clock
that resets the activity in each of its parallel systems. His experiments showed,
for very brief exposures to the stimulus, that we perceive color 40 ms before we perceive
form and 80 ms before we perceive motion. Thus, in the visual system color, form and
motion are processed independently resulting in an asynchronous behavioral output
from each independently. In other words, under these circumstances, there is no “binding”
process involved in visual perception at this level. However, for longer exposures,
and in normal on-going perception, this effect is not seen, and the color, shape and
movement of an object are seen as bound together. The reason for this difference is
not at present understood (Zeki, 2015). To explain why this asynchronization is seen
with, and only with, very short stimulus exposures, we can suggest that three visual
pathways (color, shape and motion) above are faster than the claustral pathway (2)
listed above that carries the information that there is an object out there. Consequently,
for very brief stimulus exposures, there is not enough time for pathway 2 to deliver
its message—so “binding” cannot be completed. This suggests that experiments could
be done to monitor the bioelectrical activity of object cells during the rat's perception
of objects.
Thirdly, employing advanced multivoxel fMRI pattern analysis techniques, Erez et al.
(2015) have produced strong evidence that the construction of the form of visual phenomenal
objects in higher visual cortex (especially perirhinal cortex) is effected by an explicit
conjunctive coding mechanism (based on an elaborate Hubel and Wiesel's hierarchical
system). However, they did not investigate how the color and motion aspects of the
visual triad are constructed, nor how these aspects are interrelated with each other
and with the form system. So their findings are not directly relevant to the binding
problem. These experiments should be repeated and adapted in a study of interactions
between form, color and motion.
Fourthly, Baizer et al. (2014) have found structural discontinuities in the anatomical
structure of the claustrum that is minimal in some primates but marked in cetaceans.
The authors conclude that this fact argues against the hypothesis put forward by Crick
and Koch (2005) and by Smythies et al. (2012) that intraclaustral processing of information
is important. Instead, they suggest that each functional subdivision of the claustrum
simply contributes to the function of its cortical partner. However, it can be argued
that their technique only reveals where the claustral neurons are located, not how
they are interconnected. In particular their hypothesis fails to account for the extensive
evidence that the claustrum functionally interconnects many systems (Minciacchi et
al., 1985; Zhang et al., 2001; Nunn et al., 2002; Emrich et al., 2006; Kavounoudias
et al., 2008; Remedios, 2012; Ishizu and Zeki, 2013). In particular Torgerson et al.
(2015) recently reported that network theoretical analyses show that the claustrum
is a primary contributor to global brain network architecture especially between the
frontal lobe and cingulate regions. They conclude that this shows that the claustrum
functions as the putative “gate keeper” of neural information for consciousness awareness.
It is possible that the new data by Jankowski and O'Mara might answer Zeki's question.
If the information—that the experiences of color, shape and movement of a visual object
come from one single object—is not supplied by synchronization of the direct sensory
input, might it be supplied instead by activation of particularly located “object”
neurons in the claustrum (and other “object” responsive neurons in related cortex)?
The “object” neurons might play the role in modulating spatially guided behavior in
the manner suggested by Jankowski and O'Mara (2015) and also, in addition, play a
role in “binding.” This entails that —
During the visual perception of an object, the information as to the particular properties
of that object (i.e., its color, shape and movement) is transmitted in parallel and
processed independently in the three pathways concerned as Zeki (2015) reports—with
little “cross talk” (Orman, 2015). This lack of cross-talk entails that the system
gets no information that these stimuli come from a single object and
The information that these messages originate in a single object is carried in parallel
by the claustral object neuron system operative in that particular location.
My hypothesis involving object neurons in the claustrum has close relations to the
Visual Index Theory put forward by Pylyshyn (2001). In that, he suggests that, in
perception and cognition, the brain does not operate primarily by noting first the
properties of objects and then coordinating these into objects. He suggests instead
that, in real life, information access to the visual world (attention) is allocated
first mainly, but not entirely, to objects. This involves the primary detection and
tracking of objects. He says:
“It may be that we detect objecthood first and determine location the way we might
determine color or shape—as a property associated with the detected objects. If this
is true then it raises some interesting possibilities concerning the nature of the
mechanisms of early vision. In particular, it adds further credence to the claim that
we must have a way of referring directly to primitive visual objects without using
a unique description under which that object falls.”
The discovery of object neurons in the claustrum may well have implications for Pylyshyn's
theory.
More evidence relating to the role of synchronized oscillations in neurocomputation
has been provided by studies of the McGurk effect. This effect is a species of audio-visual
speech sensory integration in which similar, but subtly different, phonemes are presented
by the auditory and visual routes. The result is that a third phoneme intermediate
between these two is actually heard. In McGurk-negative people this process is faulty
and the subject experiences two different phonemes by the auditory and visual routes
that do not blend. Fingelkurts et al. (2003) have studied this phenomenon by the brain
operational activity EEG/MEG technique. This yields information about the level of
synchrony in the different brain operations involved. These workers define multisensory
integration in this instance as an emergent process, which combines unimodal signals
into a new multimodal representational percept. They showed that the McGurk effect
in normal people is accompanied by moment-to-moment metastable synchronization in
the beta and alpha ranges of the on-going changes of brain. Moreover, in McGurk-negative
subjects this synchronization is actively suppressed. Unfortunately there is no currently
information whether alpha and/of beta range EEG activity operates in the claustrum.
One hypothesis re “binding,” that has been widely supported, is that gamma oscillations
provide a “clock” for precise temporal encoding and “binding” of signals about stimulus
features across brain regions. To test this Burns et al. (2011) computed phase and
frequency trajectories of gamma-band bursts, using time-frequency analysis of LFPs
recorded in macaque primary visual cortex (V1) during visual stimulation. The authors
define the term “clock” to indicate a signal that supplies a regular deterministic
structure for time-dependent computation. Their data were compared with simulations
of random networks and clock signals in noise. The authors report that gamma-band
bursts in LFP data were statistically indistinguishable from those found in filtered
broadband noise. They concluded that V1 local field potential data did not contain
clock-like signals. However, they suggest that a noisy gamma signals could still perform
timing functions in neurocomputation. This system could act as a resonant stochastic
filter that could operate as a transient synchronizing pulse that could synchronize
different gamma-activated networks to fire simultaneously.
If the “low” level action of the claustrum in binding the visual input is carried
out by the action of “object” neurons rather than by integrating gamma oscillations,
then the action of the mechanism we have proposed for the integrative action may be
limited to the “high” level that refers to the postulated competitive interactions
at the highest sensorimotor level of synchronized oscillations in multisensory, cognitive
and limbic cortico-claustral circuits for access to the executive motor cortex (Smythies
et al., 2012, 2014) in the control of voluntary behavior. For example, during a piano
recital, the pianist's brain needs constantly and dynamically to integrate complex
auditory, visual, somatosensory, and limbic signals and motor instructions so that
she can produce a smooth flow of music. The claustrum may play a key role in this
process.
Conflict of interest statement
The author declares that the research was conducted in the absence of any commercial
or financial relationships that could be construed as a potential conflict of interest.