The Adaptable Mind: What Neuroplasticity and Neural Reuse Tell Us about Language and Cognition - John Zerilli 2021
Cortical Map Plasticity
Aspects of Neuroplasticity
2.4.1 Intramodal plasticity
The most convincing evidence of cortical map plasticity comes from studies of plastic changes to adult primary sensory cortices. Sensory cortical areas relating to touch, vision and hearing “all represent their respective epithelial surfaces in a topographic manner” (Buonomano & Merzenich 1998, p. 152). This means neighboring cortical areas respond to neighboring sensory receptors. Somatosensory cortex maps areas of the skin’s surface somatotopically such that “neighboring cortical regions respond to neighboring skin sites.” Likewise, auditory cortices map tones tonotopically, and visual cortices map features of the visual field retinotopically. Close to three decades of research now confirm the potential for these sensory cortices, and their somatotopic, tonotopic, and retinotopic coordinates to undergo plastic changes in a use-dependent manner (Buonomano & Merzenich 1998, p. 152).
The plastic changes in view here could well include the recovery of function after injury to the cortex; for example, language cross-lateralization following trauma (Polger 2009, p. 464; Clark 2009, p. 365). In such cases, a certain psychological function, be it tactile, visual, auditory, motor, or linguistic, is mediated by a specific region of cortex at time t1, and by a different region of cortex at time t2 (Polger 2009, p. 464). A particularly striking example of this is seen in the case of children who develop normal or nearly normal language abilities after a left hemispherectomy, in which the left cerebral hemisphere (which typically mediates language) is either disabled or removed in its entirety (Laurence & Margolis 2015, p. 123). A child known as “EB” was found to have recovered most of his language skills two years after undergoing a left hemispherectomy at the age of two and a half and tested as virtually normal with respect to linguistic ability at age 14, his language faculty now subserved by regions in his right hemisphere (Danelli et al. 2013).
While such instances of plasticity are certainly impressive and reveal that the phenomenon is not confined to sensorimotor cortices alone, more typical examples (indeed, the first to be discovered) involve the expansion of cortical maps to neighboring regions of intact cortex that have been deprived of sensory input from within the same modality as that subserved by the invading cortex, such as might occur when the cortical area corresponding to one manual digit invades the neighboring area corresponding to the adjacent digit following a loss of input to the adjacent digit (Rauschecker 2001). This phenomenon is known as “intramodal” plasticity. The earliest studies of neuroplasticity reported intramodal effects in adult monkeys. Using the topographically arranged somatosensory cortical map as the dependent variable, it was found that when deprived of input, either by median nerve transection or digital amputation, though initially unresponsive, the somatosensory map did not remain unresponsive and was soon activated in response to adjacent inputs (22 days in the case of transection, two to eight months in the case of amputation). Similar results were reported after denervation or amputation in the raccoon, flying fox, cat, and rat, and “large-scale remodeling can occur in human somatosensory and motor cortical areas in the weeks or months immediately following limb amputation” (Buonomano & Merzenich 1998, pp. 163, 165). The results are equally dramatic for the visual and auditory cortices, demonstrating that, “when a given cortical area is deprived of its normal afferent inputs, it reorganizes so that the deprived area becomes responsive to sensory inputs formerly represented only within the cortical sectors surrounding those representing lesioned input sources” (Buonomano & Merzenich 1998, p. 167).
It is as well to note that intramodal plastic changes may be induced without sensory deprivation. Studies on somatosensory, visual, and auditory cortices show that intramodal plastic changes can be induced by training animals on specialized tasks. In humans, magnetoencephalography (MEG) reveals that hand representations of Braille readers are significantly larger for the right index finger than for the left index finger or for the right index finger of non—Braille readers (Pascual-Leone & Torres 1993). Likewise, the digital representation of string players is larger for the left hand than for the right hand or the left hand of control subjects (Elbert et al. 1995).
2.4.2 Crossmodal plasticity
Whereas intramodal plasticity (as its name suggests) occurs within a modality, “crossmodal” reorganization involves “expansion of maps in one modality as a result of deprivation in another” (Rauschecker 2001, p. 244). The changes here are more obviously compensatory. Cortical maps used for, say, hearing, might project into occipital cortex following deprivation of visual stimuli, whereupon occipital cortex acquires the processing structures typical of auditory cortex; or visual deprivation might lead to recruitment of primary visual cortex for tactile processing (Noppeney 2007). And since the area supporting the lost function is put to an alternative use, crossmodal plasticity actually makes recovery of the original function quite challenging (Pascual-Leone et al. 2005, p. 395). While it had previously been supposed that interventions must be drastic to induce crossmodal plastic changes, “it is now clear that simply withholding the normal pattern of sensory experience in one modality is sufficient to reorganize the neural representation of the remaining senses”; furthermore, “[i]t appears that the same synaptic mechanisms are invoked that also rule synaptic changes within the same modality” (Rauschecker 2001, pp. 244—245). Crossmodal changes require that cortical maps receive input connections, albeit indirectly, from new epithelial surfaces, and there are essentially two ways for this to occur: either via synaptogenesis, in which new connections are established between the deprived cortical region and a region that already has the relevant connections to the sensory end-organ; or the “unmasking” (strengthening/rearrangement/potentiation) via LTP or some other synaptic plastic mechanism of existing connections between the deprived cortex and the sensory end-organ and/or its associated cortex (Rauschecker 2001, p. 255; Ptito, Kupers, et al. 2012). Unmasking is probably preliminary to synaptogenesis (Pascual-Leone et al. 2005, pp. 379, 394—395; Merabet & Pascual-Leone 2010, p. 48). There is experimental support for both mechanisms in crossmodal plasticity, and both are likely to play a role in intramodal plasticity.
The extent of crossmodal plastic change is of course partly a function of time (Noppeney 2007). Short-term changes that enhance the processing capabilities of spared modalities are probably the effects of unmasking and consequently more readily reversible after input restoration (Pascual-Leone et al. 2005, pp. 390—391; Noppeney 2007, p. 1177). Blindfolding induces rapid changes that are just as swiftly reversed after visual input restoration. Long-term deprivation, on the other hand, is more likely to result in sustained structural reorganization through synaptogenesis following initial unmasking (Pascual-Leone et al. 2005, pp. 390—391). This would no doubt explain why the most dramatic crossmodal impacts are observed in cases of early-onset and congenital blindness: “functional reorganization is particularly pronounced in early onset blindness” (Noppeney 2007, p. 1170). The occipital cortices of such subjects, for instance, appear to be functionally important for Braille character identification (although not detection), suggesting a functional contribution of the reorganized occipital cortices in complex tactile discrimination (Noppeney 2007, pp. 1173—1174). Early and congenitally blind subjects routinely outperform sighted subjects in both episodic and semantic memory tasks and may even require the occipital pole for higher-level cognitive and semantic processing (Noppeney 2007, pp. 1171, 1174).
2.4.3 Supramodal (or “metamodal”) organization
Not only congenitally and early-blind subjects, but sighted subjects, too, have been found to exhibit occipital cortex activation during nonvisual information processing (Leo et al. 2012, p. 2). The activation in such cases, however, is not straightforwardly crossmodal, since it requires neither sensory deprivation nor special training. While any activation of occipital cortices in sighted subjects performing nonvisual tasks might be ascribed to a preference for visualizing nonvisual afferents, the same response pattern in congenitally blind subjects—by definition lacking vision since birth—reveals that some other principle of cortical functional organization is involved. In these cases, occipital cortices do not merely serve as the site for nonvisual information processing, as might be presumed to occur in a standard case of crossmodal plasticity, but seem to be contributing something visual to the nonvisual input, and this is no less true for blind subjects (Striem-Amit & Amedi 2014, see p. 21). That is to say, nonvisual information is apparently being processed visually, in contrast to crossmodal plasticity, which would (presumably) involve the nonvisual processing of nonvisual afferents, albeit in primary visual cortex. Evidence for the phenomenon, variously termed “supramodal,” “metamodal,” or “amodal” organization (Pascual-Leone & Hamilton 2001; Striem-Amit & Amedi 2014; Laurence & Margolis 2015), came originally from studies of the dorsal and ventral visual pathways, implicated, respectively, in space and motion discrimination and object/shape-category recognition. More recently, supramodally active regions have been confirmed beyond the occipital cortices (Leo et al. 2012, p. 2).
The nature of supramodal organization is best illustrated by studies involving early and congenitally blind subjects. The dorsal visual pathway of such subjects is active during tactile and auditory motion-discrimination tasks and reflects the activation patterns of sighted controls performing corresponding tasks (Ptito, Matteau et al. 2012, p. 2). Similarly, the ventral visual pathway of early and congenitally blind subjects is active during both haptic (tactile) and nonhaptic (electrotactile) object exploration tasks, again reflecting activations observed in sighted controls performing corresponding tasks (although blind subjects activated larger portions of the ventral stream during nonhaptic tactile shape discrimination than did sighted controls) (Ptito, Matteau et al. 2012, p. 2). In a recent study, it was shown that visual experience in the perception of body shapes is not necessary for the activation of the visual extrastriate body area (EBA) (Striem-Amit & Amedi 2014). Congenitally blind subjects were trained to use a “visual-to-auditory sensory substitution device” that converts visual images into auditory “soundscapes.” The EBA was robustly active when subjects were presented with body soundscapes. Hence, “despite the vast plasticity of the cortex to process other sensory inputs” (i.e., crossmodal plasticity), these findings suggest “retention of functional specialization in this same region” (Striem-Amit & Amedi 2014, p. 4). The dorsal and ventral processing streams, and the EBA in particular, appear to be modular, developmentally constrained, and functionally preserved, despite complete early and congenital visual impairment. That they are responsive to sensory information channeled from other modalities also suggests that these regions are not strictly domain-specific, since they are not beholden to specific sensory transduction pathways. Instead, they seem to be sensory-independent and task-selective (Striem-Amit & Amedi 2014, p. 5). The preexisting intermodal connections that are unmasked under crossmodal influence may, apparently even in the absence of crossmodal plastic unmasking, supply the critical cortical infrastructure supporting this supramodal dynamic (Pascual-Leone & Hamilton 2001, p. 439; Pascual-Leone et al. 2005, pp. 393—394; Leo et al. 2012, p. 2). The original motivation for domain specificity might have been rationalized in roughly the following way: Any module must (minimally) have a specific function it “knows” to perform on just the right occasion/s. Cognitive scientists can explain this with the suggestion that a specific input or external stimulus cues the module to respond (Pascual-Leone & Hamilton 2001, p. 431). What supramodal organization vividly demonstrates, however, is that inputs need not be external stimuli—internally mediated stimuli across modalities are normal—and that any one module will typically be sensitive to more than one stimulus, including those channeled along intermodal pathways. Put another way, it would appear that modules are frequently reused.4 I shall explain this in greater detail in Chapter 3.
Compelling evidence of supramodal organization also comes from subjects whose senses are intact. (This material does not address the kind of plasticity we have been considering so far in this chapter, but it is related in ways that will become clearer in Chapter 3, as well as Chapter 6.) It had already been known that unisensory cortices may be active when presented with stimuli coming through other modalities, as when a single stimulus component of a typically bimodal event with a close semantic connection is presented on its own; for example the sound of tools, the voice of a loved one, the sight of lips mouthing words, and such like (Hirst et al. 2012). Learning and conditioning of arbitrary pairings of unrelated stimuli may also produce these results (Hirst et al. 2012, p. 2). What was not confirmed until recently is whether these results depended on a prior semantic association, or otherwise “an explicit conditioning paradigm, or prolonged, habitual co-occurrence of bimodal stimuli” (Hirst et al. 2012, p. 2). Hirst et al.’s (2012) clinical study confirmed that, even without sensory deficits, training, or semantic associations, primary visual cortex exhibits an increased number of active neurons when presented with sounds alone, provided that subjects are pre-exposed to the auditory and visual stimuli. There is also evidence that the occipital cortex of sighted subjects is active during tactile processing of orientation, and, perhaps most astonishingly, that semantic word-generation in sighted subjects depends partly on bilateral occipital cortices, regions that have always been supposed to be among the most specialized in the brain (Pascual-Leone et al. 2005, p. 394). Studies by Antonio Damasio and Alex Martin were among the first to demonstrate activation of motor areas during verb-retrieval tasks and visual areas during noun-processing tasks, such as naming colors and animals (Damasio & Tranel 1993; Damasio et al. 1996; Martin et al. 1995, 1996, 2000). Merely the sight of manipulatable artifacts—indeed, just seeing their names—activates parts of the brain associated with prehension (Chao & Martin 2000).
The material presented in this chapter is by no means intended to serve as an exhaustive or even necessarily comprehensive account of the fascinating field of neuroplasticity. But what I have provided ought to be sufficient to support the claims I make in Chapter 6. In the next chapter, I provide a synopsis of what could well be regarded as yet another class of neuroplastic responses: responses that are, however, sufficiently distinctive in character when compared with cortical map plasticity and memory consolidation as to warrant separate consideration.