A.k.a. Form Constants in Connectomic Context: Abnormal Visuocortical Activation May Reflect Large-Scale Connectivity Alterations in Brain Functional Networks
In a widely cited paper, Ermentrout, Cowan, et al. (1978) discussed visuocortical correlates for the geometric patterns sometimes hallucinated (or pseudohallucinated) by patients experiencing simple partial (“petit mal“) seizures, migraines, and several other conditions.
The authors correlated these perceived patterns with fluctuations in resting-state electrophysiological activity in the visual cortex. However, the human visual pathway has been mapped with increasing precision over the past two decades, and it is now well understood that an interlaced sequence of structures and functional networks in the brain is associated with the processing of visuocortical activation patterns, each element of every network playing a crucial part in the analysis of and response to these signals. For example, the discovery of visuotopic (and possibly even directly retinotopic) maps in the temporal and parietal cortices – as well as the thalamic lateral geniculate nucleus (LGN) – lends weight to the idea that even visual/spatial perception itself is a multilobar process.
A logical correlate of these discoveries is that certain neurophysiological pathologies underlying visual form constants would also likely result in multimodal processing changes – and thus, perceptive changes – throughout the brain’s visual, somatosensory, associative, and cognitive processing centers.
Nevertheless, many previous studies of form constants have focused on activation patterns in the visual cortex alone. While visuocortical mapping can provide useful neural correlates for frequently observed visual patterns, the current state of research in the field of multi-scale cerebral functional networks makes it clear that an analysis of functional connectivity alterations associated with form constants is crucial to understanding the correlates and linkages of these patterns – as well as other hallucinatory and pseudohallucinatory percepts – at multiple functional and nodal scales within the human connectome as a whole. A tentative framework for such an integrative model is proposed here.
To begin, an analysis of the neural correlates for visual form constants will prove useful for comparison with other abnormal percepts.
The visual cortex, the frontal eye fields (FEF), and several other regions – including areas of the parietal and temporal lobes, as demonstrated by Slotnic (2009, 2010) and others – have been shown to render 2-dimensional visuotopic maps. However, the most directly retinotopic of these maps are found in the lower layers of the visual cortex, especially V1 (striate cortex).
In other words, straight lines in the lower visuocortical layers are mapped to lines following logarithmic spiral curves along the retina – and vice versa. By applying this function to observed patterns of visuocortical “noise,” shapes corresponding to the reported form constants can be produced.
Although the Ermentrout logarithm function predicts an isotropic map, evidence suggests that some anisotropies exist – in particular, more neuronal resources appear to be associated with vertical coordinates than horizontal ones. Nevertheless, evidence for visual forms similar to those predicted is widespread.
Ermentrout and his coauthors also discussed a related and relevant idea: that although these geometric forms themselves were likely reliant on visuocortical activity (as opposed to activation patterns in the more rostral lobes) more complex associations and expansions on the forms would involve many other cerebral areas. Models of cerebral functional connectivity at the time of the study were largely focused on modular network analysis, but more recent research has begun to contextualize form constants – and the processing centers associated with them – within a more multimodal connectomic framework.
It is to these multimodal percept alterations that we now turn. A brief explanation of larger-scale multilobar resting-state connectivity patterns will provide a useful introduction for an examination of possible neurophysiological correlates for such abnormal perceptions.
Also, as has been demonstrated by Sepulcre, Liu, et al. (2010), neurons in the retinotopic visual areas display a significant resting-state preference for local, rather than distant, functional coupling. (These functional couplings are to be distinguished from the anatomical structural networks mentioned above.) This local functional tendency is similar to preferentially local resting-state connectivity patterns found in the somatosensory, auditory and motor areas. In contrast, association cortices in the parietal, temporal and frontal lobes display a resting-state preference for distant functional coupling, in keeping with their functionality as correlative processing centers. Areas such as the posterior cingulate (PCC) and medial prefrontal (MPFC) cortices, which deal with emotional processing and self-referential cognition (respectively), display high levels of resting-state functional coupling at both local and distant ranges.
During task-positive states, however, functional connectivity networks in classification and sequencing areas – such as the inferior frontal gyrus (IFG), the inferior parietal lobule (IPL), the lateral temporal cortex (LTC), and the dorsal anterior cingulate cortex (ACC) - display an increased tendency toward local functional coupling; as do retinotopic areas of the frontal cortex. The visual cortex, by contrast, displays a heightened preference for distant functional coupling during task-positive states. This seems to imply that during task engagement, the visual cortex becomes increasingly communicative with the parietal and temporal association and orientation hubs. These areas exhibit increased associative and correlative activity, and the FEF exhibit a heightened tendency toward local pattern analysis.
These functional connectivity patterns invite comparison with connectivity abnormalities observed in several pathologies associated with form constants. Because visual form constants are known to constitute only one result of multi-scale disruptions in various functional networks, the neurophysiological nature of these disruptions bears closer examination if their full range of effects is to be understood.
Hadjikhani et al. (2001) have demonstrated that during migraines, cortical spreading depression (CSD) creates disruptions in the electrophysiological activity of the visual cortex, sometimes resulting in migraine aura: altered visual perceptions – often of geometric shapes – which may be accompanied by other sensory distortions, linguistic impairment, spatiotemporal fluctuations (altered senses of body, time, and space) and even high-level cognitive changes.
Previous research has demonstrated that while the visual and auditory disruption types reflect functional connectivity alterations in and among their respective cortices, these and other hallucinatory and pseudohallucinatory percepts are ultimately etiology-independent, and rather represent the responses of specific sensory networks (and thus, of a subjectively perceived sensory modality) to the same underlying CSD process.
For example, imaging studies of cerebral areas known to be affected by CSD activity indicate that as functional connectivity is disrupted throughout the somatosensory area, as well many areas of the temporal and parietal lobes, these areas display preferences for local functional coupling. In short, it seems likely that the form constants associated with migraine aura are but one manifestation of a multimodal hallucinatory (and/or pseudohallucinatory) pattern reflecting functional alterations across a variety of cerebral regions. However, the exact natures of the altered perceptions produced by these alterations – and the relationships of those perceptual alterations to CSD itself – present promising avenues for further research.
Functional connectivity alterations during epileptic activity have also been mapped. Temporal lobe epilepsy (TLE) is known to be associated with simple partial seizures, which often constitute preludes to seizures of the partial-complex or tonic-clonic types – all of which involve excessively expanded functional connectivity of networks throughout the temporal, parietal, and frontal lobes. Simple partial seizures are distinguished from other types primarily on the indication that the flow of consciousness is uninterrupted. Patients often report a sense of déjà vu, as well as auditory, olfactory, and visual hallucinations – including those of geometric form constants – during these seizures.
As Liao, Zhang, et al. (2010) have demonstrated, in interictal periods, the brains of patients with mesial temporal lobe epilepsy (mTLE) manifest decreased functional connectivity in the frontal and parietal lobes, and along the frontoparietal border. These regions are strongly implicated in the default mode network (DMN) and the dorsal attention network (respectively), implying that disruptions of both resting-state and task-specific connectivity during larger-scale TLE seizures may contribute to long-term functional connectivity alterations. This is consistent with the findings of Laufs, Hamandi, et al. (2007), who demonstrated that even resting-state default-mode activity was frequently interrupted and localized by small interictal epileptic discharges in TLE patients.
EEG and fMRI studies of complex-partial TLE seizures, and interictal activity in mTLE patients, provide the most thoroughly studied evidence of functional disruptions in the DMN during epileptic events. However, further research into these network fluctuations is likely to provide more precise insight into some of TLE’s more cognitive symptoms - such as hyperreligiosity and hypergraphia - and their relationship to the altered visual perceptions with which they may share a related etiology.
These pathologies provide several examples - but by no means a full range – of conditions under which alterations in functional connectivity networks may produce not only visual form constants, but multimodal hallucinations (and/or pseudohallucinations). While research has been successful in mapping neural and functional correlates for some of these percept types (especially visual and auditory aura), these findings also imply a need for further research into the relationships between pathological alterations in functional networks’ overall connectivity and the diverse range of altered somatosensory, spatial, temporal, and cognitive percepts reported by patients. Integration of this data into functional connectivity models will likely yield a more complete connectomic context for the neural processes underlying visual form constants, as well as other types of alterations in subjective perception.
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