Dateline Atlanta, SfN 2006: Hughlings Jackson vindicated again

Alvaro Pascual-Leone is so the man! Work in his lab on the plasticity of the brain’s response to sensory deprivation in blind and sighted participants has been ongoing for years, with amazing results.

Much of his work bears on the concept of unmasking, as postulated by the eminent Brtitish neurologist John Hughlings Jackson. 

Hughlings Jackson’s work was embedded in a framework of the brain as an organ with a primitive “early” core of functionality surrounded by later developed, more complex stuctures. His claim was that we could not observe the workings of more primitive brain areas as functions undertaken by more recently developed structures masked lower-level operations. Only with unmasking by brain damage could we see the primitive brain function. From, we can see these two rules named after Hughlings Jackson that establish this dictum:

Jackson’s law: Loss of mental functions due to disease retraces in reverse order its evolutionary development.

Jackson’s rule: After an epileptic attack, the nerve functions that are least developed are less affected and more rapidly recovered than the more complex ones.

Here’s the work in question (you can find the abstract on SfN’s website for the 2006 conference), by Amedi in Pascual-Leone’s lab: “Highly transient activation of primary visual cortex (V1) for tactile processing in sighted following 5 days of blindfolding” — A. AMEDI, J. CAMPRODON, L. MERABET, F. BERMPOHL, E. HALIGAN, N. BASS-PITSKEL, I. RONEN, D. KIM, A. PASCUAL-LEONE 

So, what did these authors find? When participants came into the lab they were securely blindfolded. They were given extensive tactile tasks (called the TOR tasks, for Tactile Object Recognition). Initially (Day 1), there was strong Lateral Occipital activation (LOC/LOtv) on fMRI in these people in the TOR tasks. Amir Amedi has reported this finding before.

Crucially, there was no activation of V1 (primary visual cortex) in these tactile object recognition tasks. By Day 5, after extensive training, V1 showed activation with performance of the tactile object recognition tasks in the scanner. The V1 activation started to diminish almost immediately upon removal of the blindfold and was completely gone 2 days later.

Criticisms that V1 activation after blindfolding and subsequent performance benefit on tactile tasks is epiphenomenal, and thus not required for performance of the tactile tasks (so, saying V1 activation is an imagery component to the tasks, for example), are rendered moot by Cohen’s work with blind participants and Pascual-Leone’s earlier work in which deactivating V1 with Transcranial Magnetic Stimulation disrupts newly developed skill in Braille reading.

So, deprive the brain, provide extensive experience, and there is recruitment of at least one kind of tactile processing (object recognition, and also apprehension of spacing in a tactile array, see abstract) by a primary visual area. How can this happen? Existing somatosensory connections to V1, and sparse ones at that, are used and stengthened, precisely as the unmasking idea would predict.

One relevant finding from 1999 is that for grating orientation discrimination there is substantive modulation by visual cortices (Zangaladze et al., Nature). To the lessons from these data we can now add another kind of specific tactile function performed by a primary visual region, that of determining spacing between elements, as well as a locus for more abstract tactile processing of whole objects.

We clearly show plasticity in many ways in the nervous system. Functionality is preserved at several evolutionarily-specified “levels” and this functionality can come to the fore with deprivation very quickly. One important way this is accomplished is by the rapid recruitment of already existing connections, once they are unmasked.

Here’s the full text of the abstract:

The occipital cortex undergoes dramatic cross-modal plasticity in the blind. This could reflect connectivity and processing, which exist also in sighted (but is inhibited to some extent by visual input), or massive reorganization and growth of new connections due to prolonged blindness. One approach to answer this question is to induce complete visual deprivation in sighted subjects (Pascual-Leone et al. 2001, 2005). Here we studied the effects of 5 days of blindfolding on different aspects of tactile processing. In experiment 1 we investigated tactile object recognition task (TOR) and verbal memory functions. At baseline and on Day 1, LOC / LOtv showed robust TOR activation (Amedi et al. 2001, 2005). Retinotopic areas including V1, showed negligible activation to TOR. However, on Day 5 we found robust TOR activation in V1 with either the left or the right hand but not during low-level sensorimotor controls. This activation is dramatically reduced only hours following the removal of the blindfold, and was absent 2 days later. This clearly shows a dramatic change in the V1 pattern of activation following complete visual deprivation. A similar pattern was observed in experiment 2 in which we compared distance versus roughness tactile processing of stimuli consisted of 7 tactile patterns of raised embossed dots (Braille-like stimuli, 1 mm in diameter, 2 mm in elevation and arranged in a tetragonal array with constant inter-dot spacing varying from 1 to 7 mm). Preliminary results suggest that distance more than roughness recruited early visual cortex. The speed of these functional changes makes the establishment of new connections highly improbable. Instead, we hypothesize the existence of somatosensory inputs to V1, that become unmasked with visual deafferentation.

4 responses to “Dateline Atlanta, SfN 2006: Hughlings Jackson vindicated again

  1. Do you happen to know of good sources for more info on Hughlings Jackson’s work? It seems rather interesting.

  2. First post on the schroppfy’s blog! That’s some cool stuff. Do you know if anyone has done similar studies in monkeys or other animals? I would be interested in mechanism. Presumably some sort of scaling mechanism resulting from deprivation could allow the somatosensory inputs to register above the noise. It would also be cool to see if those afferents were mostly silent (NMDAR only) before the shift and then changed, or if it’s a more simple Hebbian-ish mechanism.

  3. Grant, most of the somatosensory plasticity work is in monkeys after finger fusion or amputation (Taub would be one reference), and a lot of the work in reorganization of primary visual cortex receptive fields after retinal lesions is in Charlie Gilbert’s lab (seminal paper, invoking CaMKII mechanisms — NMDAR related, right?; see Obata S, Obata J, Das A, Gilbert CD Molecular correlates of topographic reorganization in primary visual cortex following retinal lesions. CEREB CORTEX 1999 APR-MAY;9(3):238-248). Note in some of this work there are “long range horizontal connections” being altered, but these are clearly not as long range as the kind of thalamocortical circuits that must be present here for Pascual-Leone’s reorganization to take place.

    The closest I know to an animal model is the rewiring of the ferret auditory cortex so it can “see” by Sur at MIT; there collicular inputs to cortex are damaged so that the rewiring can occur. Other than that I know of no suitable animal studies showing these duplicate inputs (by the way, spared inputs from the superior colliculus and maybe the pulvinar to V5 are said to be responsible for blindsight, so we have another human case, but notice this is still *within* a modality, so that’s why these Pascual-Leone results are so cool!).

    Neil, as far as Hughlings Jackson, I suggest googling around. He was an amazing neurologist; the first to recognize the primary role of the right hemisphere in certain types visuospatial processing, back in the early 1870s or so, and he was also perfectly spot on in realizing the right hemisphere’s role in both emotional processing and, critically, in inhibition. He was able to do all this by exceedingly careful observation (in the case of epilepsy he watched his wife’s seizures) and brilliant induction.

  4. Pingback: Are “big ideas” taught in grad school now? An appreciation of John Hughlings Jackson. | Peripersonal Space

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