It has been clear for almost two decades that cortical representations in adult animals are not fixed entities, but rather, are dynamic and are continuously modified by experience. The cortex can preferentially allocate area to represent the particular peripheral input sources that are proportionally most used. Alterations in cortical representations appear to underlie learning tasks dependent on the use of the behaviorally important peripheral inputs that they represent. The rules governing this cortical representational plasticity following manipulations of inputs, including learning, are increasingly well understood. In parallel with developments in the field of cortical map plasticity, studies of synaptic plasticity have characterized specific elementary forms of plasticity, including associative long-term potentiation and long-term depression of excitatory postsynaptic potentials. Investigators have made many important strides toward understanding the molecular underpinnings of these fundamental plasticity processes and toward defining the learning rules that govern their induction. The fields of cortical synaptic plasticity and cortical map plasticity have been implicitly linked by the hypothesis that synaptic plasticity underlies cortical map reorganization. Recent experimental and theoretical work has provided increasingly stronger support for this hypothesis. The goal of the current paper is to review the fields of both synaptic and cortical map plasticity with an emphasis on the work that attempts to unite both fields. A second objective is to highlight the gaps in our understanding of synaptic and cellular mechanisms underlying cortical representational plasticity.

/pdf/cortical-plasticity-from-synapses-to-maps-2j9eoi9428.pdf

CORTICAL PLASTICITY: From Synapses to Maps

Magnetic source imaging revealed that the cortical representation of the digits of the left hand of string players was larger than that in controls. The effect was smallest for the left thumb, and no such differences were observed for the representations of the right hand digits. The amount of cortical reorganization in the representation of the fingering digits was correlated with the age at which the person had begun to play. These results suggest that the representation of different parts of the body in the primary somatosensory cortex of humans depends on use and changes to conform to the current needs and experiences of the individual.

/pdf/increased-cortical-representation-of-the-fingers-of-the-left-4thyct1h49.pdf

Increased Cortical Representation of the Fingers of the Left Hand in String Players

This study was undertaken to document plastic changes in the functional topography of primary motor cortex (M1) that are generated in motor skill learning in the normal, intact primate. Intracortical microstimulation mapping techniques were used to derive detailed maps of the representation of movements in the distal forelimb zone of M1 of squirrel monkeys, before and after behavioral training on two different tasks that differentially encouraged specific sets of forelimb movements. After training on a small-object retrieval task, which required skilled use of the digits, their evoked-movement digit representations expanded, whereas their evoked-movement wrist/forearm representational zones contracted. These changes were progressive and reversible. In a second motor skill exercise, a monkey pronated and supinated the forearm in a key (eyebolt)-turning task. In this case, the representation of the forearm expanded, whereas the digit representational zones contracted. These results show that M1 is alterable by use throughout the life of an animal. These studies also revealed that after digit training there was an areal expansion of dual-response representations, that is, cortical sectors over which stimulation produced movements about two or more joints. Movement combinations that were used more frequently after training were selectively magnified in their cortical representations. This close correspondence between changes in behavioral performance and electrophysiologically defined motor representations indicates that a neurophysiological correlate of a motor skill resides in M1 for at least several days after acquisition. The finding that cocontracting muscles in the behavior come to be represented together in the cortex argues that, as in sensory cortices, temporal correlations drive emergent changes in distributed motor cortex representations.

https://www.jneurosci.org/content/jneuro/16/2/785.full.pdf

Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys

The cortical representations ofthe hand in area 3b in adult owl monkeys were defined with use of microelectrode mapping techniques 2-8 months after surgical amputation of digit 3, or of both digits 2 and 3. Digital nerves were tied to prevent their regeneration within the amputation stump. Suc­ cessive maps were derived in several monkeys to determine the nature of changes in map organization in the same individuals over time. In all monkeys studied, the representations of adjacent digits and pal­ mar surfaces expanded topographically to occupy most or all of the cortical territories formerly representing the amputated digit(s). With the expansion of the representations of these surrounding skin surfaces (1) there were severalfold increases in their magnification and (2) roughly corresponding decreases in receptive field areas. Thus, with increases in magnification, surrounding skin surfaces were represented in correspondingly finer grain, implying that the rule relating receptive field overlap to separation in distance across the cortex (see Sur et aI., '80) was dynamically maintained as receptive fields progressively decreased in size. These studies also revealed that: (1) the discontinuities between the representations of the digits underwent significant translocations (usually by hundreds of microns) after amputation, and sharp new discontinuous boundaries formed where usually separated, expanded digital representa­ tions (e.g., of digits 1 and 4) approached each other in the reorganizing map, implying that these map discontinuities are normally dynamically main­ tained. (2) Changes in receptive field sizes with expansion of representations of surrounding skin surfaces into the deprived cortical zone had a spatial distribution and time course similar to changes in sensory acuity on the stumps of human amputees. This suggests that experience-dependent map changes result in changes in sensory capabilities. (3) The major topographic changes were limited to a cortical zone 500-700 JIm on either side of the initial boundaries of the representation of the amputated digits. More dis­ tant regions did not appear to reorganize (i.e., were not occupied by inputs from surrounding skin surfaces) even many months after amputation. (4) The representations of some skin surfaces moved in entirety to locations within the former territories of representation of amputated digits in every

Somatosensory cortical map changes following digit amputation in adult monkeys

Little is known about the mechanisms that allow the cortex to selectively improve the neural representations of behaviorally important stimuli while ignoring irrelevant stimuli. Diffuse neuromodulatory systems may facilitate cortical plasticity by acting as teachers to mark important stimuli. This study demonstrates that episodic electrical stimulation of the nucleus basalis, paired with an auditory stimulus, results in a massive progressive reorganization of the primary auditory cortex in the adult rat. Receptive field sizes can be narrowed, broadened, or left unaltered depending on specific parameters of the acoustic stimulus paired with nucleus basalis activation. This differential plasticity parallels the receptive field remodeling that results from different types of behavioral training. This result suggests that input characteristics may be able to drive appropriate alterations of receptive fields independently of explicit knowledge of the task. These findings also suggest that the basal forebrain plays an active instructional role in representational plasticity.

https://science.sciencemag.org/content/sci/279/5357/1714.full.pdf

Cortical map reorganization enabled by nucleus basalis activity.

The organization of part of the primary somatosensory cortex was examined in anesthetized raccoons at 2, 8, or 16 weeks after the normal peripheral input to this region of cortex had been removed by amputation of the fifth digit. Electrophysiological recordings were made in and around the cortical area representing the fifth digit. Eight intact animals were used to verify that this specific area could be accurately localized on the basis of the sulci and to determine the normal response characteristics of this area. The results from nine animals with the fifth digit removed provided evidence for a gradual reorganization of the cortical area which had been functionally denervated. At 2 weeks postamputation the field was almost totally unresponsive to sensory input. At 8 weeks many sites were responsive to high intensity stimulation of rather extensive regions of the hand. At 16 weeks the cells fired more readily to peripheral stimulation than at 8 weeks and tended to have smaller, more restricted receptive fields. The location of receptive fields in this latter group suggested that the fifth digit area was taken over primarily by input from the fourth digit. The time course of this reorganization is suggestive of extensive anatomical changes either within the cortex itself or at subcortical levels.

Reorganization of raccoon somatosensory cortex following removal of the fifth digit.

Averaged evoked potentials from primary somatosensory cortex (SEPs) were recorded before and after pairing the peripheral stimuli with electrical activation of the basal forebrain (BF) in anesthetized cats. Four pulses at 400 Hz were delivered to the BF 120 ms before each cutaneous stimulus and 10 to 660 such pairings were found to produce an enlargement of the SEP in 10 of 11 animals. The average increase in amplitude of the initial peak of the SEP was 69%. The SEP remained enhanced in five of six animals that were tested an hour or more after the pairing, and in one case the SEP was tested 4.5 h after pairing without diminution. The effective BF sites were located in the substantia innominata and at the rostral pole of the globus pallidus, regions known to contain many cholinergic cell bodies. Enhancement occurred consistently only if stimulation of the BF site elicited a positive wave in the cortex at a latency of 11 to 18 ms. Repeated BF stimulation without cutaneous input did not produce a change in subsequent SEPs. The long-term changes described here may be involved in experimentally- and naturally-induced cortical reorganization.

Long-term enhancement of evoked potentials in cat somatosensory cortex produced by co-activation of the basal forebrain and cutaneous receptors.

The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex

Modification of neocortical acetylcholine release and electroencephalogram desynchronization due to brainstem stimulation by drugs applied to the basal forebrain

1. Multi-unit recordings were made from SI cortex of barbiturte-anesthetized cats. In four cats, multiple vertical penetrations were made at closely spaced intervals. In 12 cats, long surface-parallel penetrations were made in the rostrocaudal or the lateromedial directions with observations taken every 100 micron. 2. Evidence is presented suggesting that cytoarchitectonic area 3a receives input from deep receptors and area 3b receives input from cutaneous receptors. 3. Within area 3b there was an abrupt change in submodality such that the rostral portion of 3b was activated by slowly adapting (SA) afferents, while the caudal portion was activated by rapidly adapting (RA) afferents. 4. The change in modality from deep to cutaneous occurred at the 3a/3b border, but the change in submodality occurred within area 3b and there was no obvious anatomical correlate of the latter transition. 5. These data suggest that there are modality- and submodality-specific bands in register with the bands of cytoarchitecture that extend across the mediolateral dimension of primary somatosensory cortex (SI). 6. A particular receptor population (or populations) from all regions of the body delivers information to each functionally specific band--one map is found in area 3a and two are in area 3b. If this pattern holds for the rest of cat SI, then there must be additional maps of the body in cytoarchitectonic areas 1 and 2.

Douglas D. Rasmusson

Papers

Reorganization of raccoon somatosensory cortex following removal of the fifth digit.

Long-term enhancement of evoked potentials in cat somatosensory cortex produced by co-activation of the basal forebrain and cutaneous receptors.

The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex

Modification of neocortical acetylcholine release and electroencephalogram desynchronization due to brainstem stimulation by drugs applied to the basal forebrain

Organization of primary somatosensory cortex in the cat.