The Sense of Self

"Grandmother Cells", or Synchronous Discharges of Neurons?

A Monthly Podcast On Cognitive Science

Brain Rhythms: The Oscillations That Bind

The “Coming Out” of the Electrical Synapse

Samir Zeki and his colleagues have shown that even though the various attributes of a visual scene are presented simultaneously, they are not perceived at exactly the same time. Colour is perceived before the orientation of lines, which in turn is perceived before movement. The lag between the perception of colour and the perception of movement is on the order of 60 to 80 milliseconds. Zeki’s experiments on visual perception of the various properties of an object led him to suggest that an individual’s consciousness may in fact be composed of a number of micro-consciousnesses corresponding to the various levels of processing in the brain. Information would then remain unconscious until it reached a "node" in the system that rendered it conscious. Thus a human being’s consciousness would be composed of a multitude of micro- consciousnesses that were ultimately integrated into a single, more global "superconsciousness" by means of language. According to its proponents, this conception of multiple consciousnesses would allow consciousness to be understood as something that is truly decentralized, without any one centre in the brain from which consciousness springs. But other authors have objected that the very idea that each of the subsystems contains a sort of "finish line" where the stimulus suddenly becomes conscious takes us directly back to the idea of the Cartesian theatre, which has been so roundly condemned by philosophers such as Daniel Dennett.

NEURONAL ASSEMBLIES AND SYNCHRONIZATION OF BRAIN ACTIVITY

One approach to an answer would be to say that the various signals from all these different parts of the brain converge on a group of cells or even a single cell that represents this conscious perception. Indeed, though the brain has a preponderance of parallel circuits, it does display a certain form of convergence as one moves farther from the primary areas of the cortex and closer to the “associative”ones. Many such areas of convergence have been identified in the frontal cortex, the anterior temporal cortex, and the inferior parietal cortex. But neuroscientists agree that these are not sites where mental representations are stored. At most, they may contain certain “codes”that can reconstruct the fragments of activations distributed elsewhere in the sensorimotor areas of the cortex.

Likewise, it is true that there are certain neurons located at the top of the hierarchy in the visual cortex that respond specifically to faces, and even to faces seen from a certain angle. These neurons definitely help us to recognize faces, because when these neurons are destroyed by a stroke, the stroke victim develops prosopagnosia, the inability to recognize faces, even of immediate family.

But apart from a few special cases such as recognizing faces, which has always been of tremendous adaptive importance, convergence is too flimsy, inefficient, and ultimately ineffective a mechanism for unifying perceptions in the brain, and it does not seem to have been selected by evolution for this purpose (follow the link to the left).

So if there is no single place where all of the information about an object converges to become conscious, is there perhaps a single time when it does? That is the other major approach to solving the binding problem, and it seems the more promising. In this approach, broadly speaking, neurons that are active at the same time are believed to be “perceiving the same thing”. In technical terms, this approach is based on the temporal synchronization of neuronal activity.

To return to the example of the green suitcase next to the blue hat, each of these two objects will be represented by a huge assembly of neurons in the brain. Each of these assemblies will include neurons that can detect various attributes of each object, such as colour or movement, or the orientation of its lines and contours, and so on. And thus, according to this hypothesis, it is through the synchronization of the various neurons coding for the various attributes of the suitcase (N1, N2, and N3 in the figure below) that the brain obtains a coherent, unified image of this object.

As for the neurons that code for the various attributes of the hat (N4, N5, and N6), they too fire synchronously to provide a unified image of this object. But as the grey dotted line shows, they do not fire at the same time as the neurons that code for the various attributes of the suitcase. And that may be how we consciously perceive two separate objects standing out against a background that is also a separate object (and that would be represented by a third assembly of neurons), and not simply an undifferentiated amalgam of lines and colours.

Francis Crick and Christof Koch took the idea of temporal synchronization one step further by proposing that this synchronized activity, when occurring at 35 to 75 Hz (hertz, or cycles per second), may be the neuronal correlate for conscious visual perception. Their idea originated with studies done on the visual cortex of cats in the 1980s. These studies had shown that large numbers of neurons could fire at the same time at a rate ranging from approximately 35 to 75 Hz. (Neuronal activity oscillating at this frequency is commonly referred to as “gamma oscillations” or simply “40-Hz oscillations”.)

Many subsequent studies both in animals and in humans showed that this high oscillation frequency of neuronal activity is closely related to the integration of perceptions, the construction of coherent representations, and to some processes of selective attention. Crick and Koch therefore developed a theory according to which the key to conscious perception lies not solely in the synchronization of neuronal activity, but in the synchronization of neuronal activity oscillating at frequencies in the range of 35 to 75 Hz.

In summary, according to this hypothesis:

• if two neurons are oscillating synchronously in the gamma frequency range (around 40 Hz), then they are contributing to the same, conscious representation;
  
• if two neurons are oscillating synchronously outside the gamma frequency range, then they are contributing to the same representation, but it is not a conscious one (for example, the representation of an object that is in your field of vision but that you are not paying attention to);
  
• if two neurons are active but are not oscillating in regular cycles, or are oscillating in regular cycles that are not synchronized, then these neurons are representing attributes that are unbound or that are bound to different representations.

Crick and Koch also believe that these transitory neuronal assemblies oscillating at about 40 Hz do not form only in the visual cortex but may also recruit neurons throughout the cortex. In this case, the colour and shape of an object would not be the only characteristics associated with it. There would also be all sorts of other characteristics, such as odour, taste, emotional associations, and so on, all of them thus helping to form a complete conscious representation of the object observed. Here then is an elegant mechanism by which the brain might distinguish, among all the representations that it has bound, those that are conscious from those that are not.

Crick and Koch had first proposed, in the late 1980s, that synchronization of the oscillations around 40 Hz was a sufficient mechanism to ensure the emergence of a conscious perception. Shortly after the year 2000, they altered their position somewhat, stating that conscious phenomena seem to arise from a competition among various “coalitions” of neurons (see box below) in which the winning coalitions determine the content of the conscious mind at any given time. And what these authors now consider a more plausible role for the synchronization of the 40 Hz oscillations is that it might act as the mechanism by which this competition is resolved, by favouring the selection of a particular neuronal assembly. This idea of neuronal assemblies that are competing at all times is also consistent with the more recent hypothesis of the “dynamic nucleus”.

Engel and Wolf also believe in synchronization, though they consider it necessary but not sufficient to generate consciousness. In their view, the information should also enter into a form of short-term memory, a suggestion that here refers to something like a global workspace.

In short, though the the hypothesis of the synchronization of oscillations at around 40 Hz undeniably contributes something to our understanding of consciousness, it is not the final word on this subject. It has, for example, undergone further interesting developments, particularly as regards the mechanism by which the brain selects the representations that will become conscious from among all of its unconscious representations.

Some of the most interesting empirical data on neuronal activity and consciousness come from the experiments of Nikos Logothetis. By recording the activity of isolated cells in the visual cortex of macaque monkeys, Logothetis demonstrated that the activity of certain neurons could be correlated with the conscious or unconscious nature of a stimulus to which these primates were exposed. Logothetis used the same method in these experiments as was used to identify the various parts of the cortex that specialize in processing different aspects of visual stimuli (shape, colour, movement, etc.). But the discovery that the neurons in a particular part of an animal’s brain always respond to a particular property of a stimulus does not tell us whether the animal is perceiving this aspect of the stimulus consciously. We also know that many visual properties extracted by the most primary visual areas do not correspond to any conscious perception, because these neurons continue to respond even when the animal is under general anaesthesia and hence unconscious. What was original about Logothetis’s experiments was precisely that they enabled this distinction to be made between stimuli that were simply represented by neuronal activity and stimuli that were perceived consciously. To make this distinction, Logothetis used rival stimuli, that is, stimuli that had mutually exclusive interpretations—in this case, images that could be interpreted as depicting either upward movement or downward movement. With training, the monkeys in these experiments learned to indicate with their hands which direction of motion they perceived. In the MT area of the visual cortex, which is responsible for detecting movement, Logothetis then found neurons whose response fluctuated in accordance with the monkey’s learned behavioural response. For example, certain neurons responded strongly when the monkey was indicating that it was perceiving an apparent upward movement. But these same neurons were far less active when the monkey was indicating a downward movement. This discovery was important, because it clearly established that the activity of neurons in the sensory areas of the cortex does not always correspond solely to the properties of an external stimulus. For example, when we compare the trials in which a given neuron was very active with those in which it was less active, we see that absolutely nothing had changed in the external stimulus or in the general conditions of the experiment. The only difference that corresponded to the change in the activity of this neuron was the perceived movement that the monkey reported by means of a behavioural response that it had learned previously. Some people might argue that the activity of these neurons merely accompanied the motor output of this behavioural response. But the location and connectivity of these neurons makes this hypothesis difficult to sustain. This type of experiment on the activity of isolated neurons thus seems to show a direct effect of higher-order attention processes on sensory processing centres. But whether the activity of these neurons in the MT area constitutes the neuronal correlate of consciousness of movement all on its own remains an open question.