Guiding Plasticity: Another Route for the Neuroscience of Consciousness

 Guiding Plasticity: Another Route for the Neuroscience of Consciousness

David Fischer

            The issue of consciousness remains an excruciatingly intricate topic for philosophers and scientists alike, in large part because of the complexity involved in merely defining it. Colloquially, the term is used in a myriad of ways, where its referents can include a state of “full presence,” awareness of one’s surroundings (i.e., not asleep), self-awareness, experience (e.g., the “redness” of our perception of red), or simply the opposite of unconsciousness. The ubiquity and ambiguity of the term “consciousness” alone problematizes its scientific pursuit, making it difficult to operationalize and hindering coherent dialogue between different groups of researchers. Some of the most successful attempts at discovering the neural basis of consciousness have articulated a particular, if not comprehensive, feature of consciousness to explain. For example, the study conducted by Schurger and colleagues (2010), found that perceiving an image consciously causes more reproducible neural patterns than when an image is perceived subconsciously (1). While the perception of images hardly captures the nuances of consciousness, it offers a tenable route of empirical investigation. Additional avenues for studying the neuroscience of consciousness may be gained through observing similarly tangible neurological events. Just as the neuroscience of consciousness requires the integration of philosophy, psychology and biology, an interdisciplinary approach within neuroscience may offer an additional route for investigating consciousness. In particular, the phenomenon of neural plasticity provides one such potential avenue for characterizing the neural basis of consciousness.

When someone suffers damage to a brain area, the central nervous system has a remarkable capacity to “relocate” the functions of that area to other brain regions through a series of neural changes – a process generally referred to as plasticity. For example, when a stroke destroys Broca’s area – a region strongly implicated in linguistic functions – the afflicted patients often find ways of recuperating language in circuitry not usually associated with language. One study demonstrated that, as patients who suffered lesions to Broca’s areas regained the ability to speak through music therapy, the circuitry formerly involved in music processing became strengthened; specifically, the white matter tracts thought to underlie the production of melody increased in size (2). This finding contributes tangible evidence to a phenomenon that could have been inferred a priori: following the complete destruction of neural circuitry associated with certain functions, the recovery of those functions must occur through neural changes that occur outside that lesioned circuitry (i.e., plasticity).

This type of plasticity pervades many cases of functional relocation: for example, blind people have been shown to recruit their occipital lobe – a region generally associated with visual processes – while perceiving tactile stimuli (3). Moreover, these instances of neural plasticity can work in reverse. One study implanted a probe into the region of a monkey’s motor cortex associated with arm movements (4). The researchers then had the monkey move a joystick with that arm. The information gathered from the motor cortex dictated the movement of a cursor on the screen; the movement of the joystick was merely a redundant mechanism. Eventually, the monkey “learned” that it no longer needed to move its arm in order to control the cursor – it could do so only through its motor cortex – and continued moving the cursor without moving its arm. Thus, plasticity can also dissociate circuitry: the monkey continued to activate its motor cortex while ceasing to move its arm, implying a separation between the motor cortex and efferent motor neurons.

So what does plasticity have to do with consciousness? The relevance of consciousness becomes most apparent in how these phenomena are explained. How are these forged associations and dissociations, mediated by neural plasticity, guided? In other words, what determines that the function of speech should be incorporated into musical circuitry, or that the motor cortex no longer needs to signal the arms in order to move a cursor? It seems that consciousness may play a substantial role in determining these connections.

While the question of what guides neural plasticity has yet to be tested, one might imagine several potential mechanisms. Let us take the recuperation of speech in musical circuitry, following a lesion to Broca’s area, as an example to be explained. Many of these possibilities rely on an assumption of necessary causality: for any neuron to become active, it must be stimulated by other cells or by internal (e.g., genetic) stimuli. Assuming this premise, we can reasonably conclude that there must be some "upstream" input – or in other words, causal stimulation – that inspires activation in Broca's area, which ultimately results in the production of speech. When someone relocates their speech function to, say, their musical circuitry, it seems equally reasonable to conclude that the upstream input that normally activated Broca’s area now causes enhanced activation in the musical circuitry. It should be noted that this type of description may be overly confident in the regional specificity of function; it is likely that speech is a function distributed much more broadly across neural circuits. However, Broca’s area has been shown to exhibit consistent activation during speech, and its destruction often strongly inhibits speech production. Therefore, for the purposes of the current description, at least some regional specificity of language will be assumed.

The question then becomes: what allows this transition to occur? One possibility is that the upstream input always had a latent connection to that musical circuitry, but after the loss of Broca's area, these connections were strengthened or "unveiled". However, it is difficult to explain how that might occur. If the musical circuitry was always activated by upstream input that causes speech, then that circuitry should receive an equal amount of synaptic input before and after the insult to Broca's area. If this is so, why would there be a strengthening of these connections afterwards? Synaptic connections are generally strengthened by an increase in usage (e.g., through long-term potentiation). What would reinforce circuitry whose activation was not altered after the insult to Broca’s area?

One might argue that perceptual feedback can account for this guidance. In other words, a stroke patient might perceive himself communicating musically after music therapy, and the rewarding nature of that perception affirms and reinforces the connections from upstream input to the musical circuitry. In fact, the researchers who conducted the study on the brain-machine interface (BMI) in the monkey described their results in a similar manner:

All together, these physiological changes suggest that as animals learn to operate the BMI during brain control, visual feedback signals representing the goal of movement, rather than information about arm movements per se, become the main guiding signal to the cortical neurons that drive the BMI. Thus, we hypothesize that, as monkeys learn to formulate a much more abstract strategy to achieve the goal of moving the cursor to a target, without moving their own arms, the dynamics of the robot arm (reflected by the cursor movements) become incorporated into multiple cortical representations. (p 205; 4)

Thus, researchers have indeed proposed the possibility that perceptual feedback can account for the guidance of neural plasticity. But is this a feasible explanation? In the case of speech relocation, how could a rewarding perception of sound reinforce speech circuitry in particular? In the case of the BMI, how could a perception possibly encode goal-directed behavior, at least on a mechanistic enough level to explain the dissociation of specific circuitry? It is difficult to imagine how perceptions could cause the appropriate kind of reinforcement. The “winner takes all” model offers an additional explanation for how circuitry might be unveiled: it is possible that Broca’s area sent inhibitory fibers to the musical circuitry, and once Broca’s area was destroyed, the connections from the upstream input to the musical circuitry were disinhibited. However, given the vast number of possible regions to which a given function might be relocated, an enormous number of such inhibitory connections would have to exist. Moreover, this model does not help explain instances of plasticity that dissociates circuitry in the absence of lesions (e.g., in the BMI). 

Yet another possibility for how plasticity processes are guided involves the redirection of axons. Perhaps the fibers that originally connected the upstream input to Broca's area must now, at risk of dying off, find other dendrites with which to form synapses. These fibers form new synapses with the musical circuitry, thereby strengthening the connection between the upstream input and the musical circuitry. However, this mechanism faces the same problems as the unveiling mechanism: How would the fibers be able to find the musical circuitry versus any other available synapses? Moreover, what would reinforce these connections while eliminating errant connections (e.g., perhaps the upstream input fibers might synapse on the somatosensory cortex, causing a tactile sensation whenever we wanted to speak)? The explanation of sensory feedback seems equally faulty: how could we go about identifying the physical underpinnings of this reinforcing/eliminating feedback “force” produced by perception? How could the rewarding aspects of perception alone account for the refinement of growth for these particular neurons?

The mechanisms proposed to guide neural plasticity seem inadequate to describe the phenomenon. It is not clear how perceptual information itself could reinforce or eliminate particular neural connections. Rather, it seems much more likely that the relationship between perception (a function that makes one aware of his actions) and neural guidance (a fine neural process) is mediated by a third factor: consciousness. Indeed, the means by which an entity establishes or dissociates neural circuitry can aptly be described as a process of consciousness: When a patient tries to speak through music, as in music therapy, the successful relocation of linguistic function comes about as the result of intentional and deliberate (or in other words, conscious) attempts. When the monkey decided to no longer move its arm to direct the cursor, it made a conscious decision to do so. Presumably its arm – controlled by the somatic nervous system – did not fall limply to its side, but rather was consciously removed from the joystick. Thus, these instances of plasticity reflect the fundamental interplay of consciousness. Moreover, given the highly mechanistic character of neural plasticity, examples such as these may offer valuable insight into a mechanistic basis of consciousness. Future research may investigate consciousness by monitoring how plasticity is guided: the answer to this question may ultimately shed light upon the neuroscience of consciousness.

Unfortunately, this suggestion does not help resolve the diversity of meaning associated with consciousness – a diversity that, as described earlier, has problematized its empirical study. Rather, this suggestion only adds yet another possible meaning of consciousness – as the guidance of neural plasticity during conscious attempts to relocate function – to the already scattered literature. However, there are several benefits to this avenue of research that perhaps merit producing an additional definition of consciousness. For one, as has been explained, breaking down the abstract phenomenon of consciousness into smaller distinct bits may offer a feasible starting point for empirical study. While the guidance of plasticity might not comprehensively explain every feature of consciousness, it provides a manageable point of entry for research. Secondly, implicating consciousness in neural plasticity may help address the elusive question of what guides these changes during intentional attempts to relocate function. Although often brushed aside as a matter of perceptual feedback, the unresolved mechanism of functional plasticity may be better understood through an investigation of consciousness.

Finally, although this direction for future research adds an additional, unneeded definition of consciousness, this operationalization of consciousness may already underlie previous definitions and findings. For example, Schurger and colleagues (2010) found that the conscious perception of images was accompanied by more reproducible neural patterns – or in other words, produced neural activity that followed more defined paths, as opposed to the more diffuse activation produced by the subconscious perception of images. The researchers suggest that the specificity of neural activation may therefore underlie conscious activity. This finding might partially account for the aspect of consciousness at play during functional relocation: the particularity of the neural pathways activated during a conscious experience might help to redefine preexisting pathways in the case of plasticity. For example, during musical therapy, stroke patients would consciously attempt to recuperate language through music. During the process, their remaining speech circuitry (i.e., the remaining upstream input) and musical circuitry would be active in a more specific and reproducible way, perhaps allowing the two particular circuits to connect. As opposed to subconscious processing, during which circuits are activated diffusely, conscious processing would produce the specificity necessary for fine changes in neural patterns.

            Thus, the phenomenon of plasticity may offer an additional means of investigating the neuroscience of consciousness. While the guidance of plastic changes may not encapsulate the entirety of consciousness, it offers a reasonable starting point and even fits in with models of consciousness previously discovered. Notably, this avenue of research was gathered from other spheres of neuroscience, specifically the study of plasticity and strokes. It may be the case that progress in the neuroscience of consciousness will require such an expansion into alternative approaches to neuroscience. It is the inherently interdisciplinary nature of consciousness – even within neuroscience, consciousness so strongly pervades so many disparate functions of the nervous system – that makes it such an elusive target for research, and yet such a crucial factor in understanding the biology of the mind.

Thank you to Professor Grobstein and the Haverford and Bryn Mawr students of the 2010 Neural and Behavioral Sciences seminar for their help in formulating the ideas of this paper.

References

1. Schurger, A., Pereira, F., Treisman, A. & Cohen, J.D. (2010). Reproducibility distinguishes conscious from nonconscious neural representations. Science, 327, 97-99.
2. Schlaug, G., Marchina, S., Norton, A. (2009). Evidence for plasticity in white-matter tracts of patients with chronic Broca’s aphasia undergoing intense intonation-based speech therapy. Ann. N.Y. Acad. Sci., 1169, 385-394.
3. Sadato, N., Pascual-Leone, A., Grafman, J., Ibanez, V., Deiber, M., Dold, G. & Hallett, M. (1996). Activation of the primary visual cortex by Braille reading in blind subjects. Nature, 380, 526-528.
4. Carmena, J.M., Lebedev, M.A., Crist, R.E., O’Doherty, J.E., Santucci, D.M., Dimitrov, D.F., Patil, P.G., Henriquez, C.S. & Nicolelis, M.A.L. (2003). Learning to control a brain-machine interface for reaching and grasping by primates. PLoS Biol, 1(2), 193-208.