Towards a unified neural mechanism for reactive adaptive behaviour

Surviving in natural environments requires animals to sense sudden events and swiftly adapt behaviour accordingly. The study of such Reactive Adaptive Behaviour (RAB) has been central to a number of research streams, all orbiting around movement science but progressing in parallel, with little cross-field fertilization. We first provide a concise review of these research streams, independently describing four types of RAB: (1) cortico-muscular resonance, (2) stimulus locked response, (3) online motor correction and (4) action stopping. We then highlight remarkable similarities across these four RABs, suggesting that they might be subserved by the same neural mechanism, and propose directions for future research on this topic

Local spatial analysis: an easy-to-use adaptive spatial EEG filter

Spatial EEG filters are widely used to isolate event-related potential (ERP) components. The most commonly used spatial filters (e.g., the average reference and the surface Laplacian) are "stationary." Stationary filters are conceptually simple, easy to use, and fast to compute, but all assume that the EEG signal does not change across sensors and time. Given that ERPs are intrinsically nonstationary, applying stationary filters can lead to misinterpretations of the measured neural activity. In contrast, "adaptive" spatial filters (e.g., independent component analysis, ICA; and principal component analysis, PCA) infer their weights directly from the spatial properties of the data. They are, thus, not affected by the shortcomings of stationary filters. The issue with adaptive filters is that understanding how they work and how to interpret their output require advanced statistical and physiological knowledge. Here, we describe a novel, easy-to-use, and conceptually simple adaptive filter (local spatial analysis, LSA) for highlighting local components masked by large widespread activity. This approach exploits the statistical information stored in the trial-by-trial variability of stimulus-evoked neural activity to estimate the spatial filter parameters adaptively at each time point. Using both simulated data and real ERPs elicited by stimuli of four different sensory modalities (audition, vision, touch, and pain), we show that this method outperforms widely used stationary filters and allows to identify novel ERP components masked by large widespread activity. Implementation of the LSA filter in MATLAB is freely available to download.NEW & NOTEWORTHY EEG spatial filtering is important for exploring brain function. Two classes of filters are commonly used: stationary and adaptive. Stationary filters are simple to use but wrongly assume that stimulus-evoked EEG responses (ERPs) are stationary. Adaptive filters do not make this assumption but require solid statistical and physiological knowledge. Bridging this gap, we present local spatial analysis (LSA), an adaptive, yet computationally simple, spatial filter based on linear regression that separates local and widespread brain activity (https://www.iannettilab.net/lsa.html or https://github.com/rorybufacchi/LSA-filter)

Pain outside the body: defensive peripersonal space deformation in trigeminal neuralgia

Perception of space has been guiding effective therapeutic interventions in a number of unilateral chronic pain conditions. However little is known about how trigeminal neuralgia (TN), a condition in which trigeminal stimulation triggers paroxysmal facial pain, affects defensive peripersonal space (DPPS), the portion of space surrounding the body within which defensive responses are enhanced. Given that TN is unilateral, in TN patients the DPPS of the face might not be horizontally symmetric as in pain-free individuals, but instead larger around the affected side. We tested this a priori hypothesis by measuring the proximity-dependent modulation of the hand-blink reflex. Stimuli delivered to the hand ipsilateral to TN elicited a stronger blink, particularly when it was measured from the eye ipsilateral to TN and the hand was closer to the face. Geometric modelling revealed (1) that DPPS was larger on the side of space ipsilateral to TN, and (2) this asymmetry was consequent to an increased estimated potential of sensory events to cause harm when they occur ipsilaterally to TN. These observations demonstrate that neural mechanisms underlying body protection in TN are adjusted to reduce the likelihood that external events evoke the painful paroxysm typical of this condition

Cortico-spinal modularity in the parieto-frontal system: a new perspective on action control

: Classical neurophysiology suggests that the motor cortex (MI) has a unique role in action control. In contrast, this review presents evidence for multiple parieto-frontal spinal command modules that can bypass MI. Five observations support this modular perspective: (i) the statistics of cortical connectivity demonstrate functionally-related clusters of cortical areas, defining functional modules in the premotor, cingulate, and parietal cortices; (ii) different corticospinal pathways originate from the above areas, each with a distinct range of conduction velocities; (iii) the activation time of each module varies depending on task, and different modules can be activated simultaneously; (iv) a modular architecture with direct motor output is faster and less metabolically expensive than an architecture that relies on MI, given the slow connections between MI and other cortical areas; (v) lesions of the areas composing parieto-frontal modules have different effects from lesions of MI. Here we provide examples of six cortico-spinal modules and functions they subserve: module 1) arm reaching, tool use and object construction; module 2) spatial navigation and locomotion; module 3) grasping and observation of hand and mouth actions; module 4) action initiation, motor sequences, time encoding; module 5) conditional motor association and learning, action plan switching and action inhibition; module 6) planning defensive actions. These modules can serve as a library of tools to be recombined when faced with novel tasks, and MI might serve as a recombinatory hub. In conclusion, the availability of locally-stored information and multiple outflow paths supports the physiological plausibility of the proposed modular perspective

Nociceptive-Evoked Potentials Are Sensitive to Behaviorally Relevant Stimulus Displacements in Egocentric Coordinates.

Feature selection has been extensively studied in the context of goal-directed behavior, where it is heavily driven by top-down factors. A more primitive version of this function is the detection of bottom-up changes in stimulus features in the environment. Indeed, the nervous system is tuned to detect fast-rising, intense stimuli that are likely to reflect threats, such as nociceptive somatosensory stimuli. These stimuli elicit large brain potentials maximal at the scalp vertex. When elicited by nociceptive laser stimuli, these responses are labeled laser-evoked potentials (LEPs). Although it has been shown that changes in stimulus modality and increases in stimulus intensity evoke large LEPs, it has yet to be determined whether stimulus displacements affect the amplitude of the main LEP waves (N1, N2, and P2). Here, in three experiments, we identified a set of rules that the human nervous system obeys to identify changes in the spatial location of a nociceptive stimulus. We showed that the N2 wave is sensitive to: (1) large displacements between consecutive stimuli in egocentric, but not somatotopic coordinates; and (2) displacements that entail a behaviorally relevant change in the stimulus location. These findings indicate that nociceptive-evoked vertex potentials are sensitive to behaviorally relevant changes in the location of a nociceptive stimulus with respect to the body, and that the hand is a particularly behaviorally important site

Ultralow-frequency neural entrainment to pain

Nervous systems exploit regularities in the sensory environment to predict sensory input, adjust behavior, and thereby maximize fitness. Entrainment of neural oscillations allows retaining temporal regularities of sensory information, a prerequisite for prediction. Entrainment has been extensively described at the frequencies of periodic inputs most commonly present in visual and auditory landscapes (e.g., >0.5 Hz). An open question is whether neural entrainment also occurs for regularities at much longer timescales. Here, we exploited the fact that the temporal dynamics of thermal stimuli in natural environment can unfold very slowly. We show that ultralow-frequency neural oscillations preserved a long-lasting trace of sensory information through neural entrainment to periodic thermo-nociceptive input as low as 0.1 Hz. Importantly, revealing the functional significance of this phenomenon, both power and phase of the entrainment predicted individual pain sensitivity. In contrast, periodic auditory input at the same ultralow frequency did not entrain ultralow-frequency oscillations. These results demonstrate that a functionally significant neural entrainment can occur at temporal scales far longer than those commonly explored. The non-supramodal nature of our results suggests that ultralow-frequency entrainment might be tuned to the temporal scale of the statistical regularities characteristic of different sensory modalities

Muscular effort increases hand-blink reflex magnitude.

Defensive motor responses elicited by sudden environmental stimuli are finely modulated by their behavioural relevance to maximise the organism's survival. One such response, the blink reflex evoked by intense electrical stimulation of the median nerve (Hand-Blink Reflex; HBR), has been extensively used to derive fine-grained maps of defensive peripersonal space. However, as other subcortical reflexes, the HBR might also be modulated by lower-level factors that do not bear direct relevance to the defensive value of blinking, thus posing methodological and interpretive problems. Here, we tested whether HBR magnitude is affected by the muscular effort present when holding the hand in certain postures. We found that HBR magnitude increases with muscular effort, an effect most likely mediated by the increased corticospinal drive. However, we found strong evidence that this effect is substantially smaller than the well-known effect of eye-hand proximity on HBR magnitude. Nonetheless, care should be taken in future experiments to avoid erroneous interpretations of the effects of muscular effort as indicators of behaviour relevance

Brain Responses to Surprising Stimulus Offsets: Phenomenology and Functional Significance

Abrupt increases of sensory input (onsets) likely reflect the occurrence of novel events or objects in the environment, potentially requiring immediate behavioral responses. Accordingly, onsets elicit a transient and widespread modulation of ongoing electrocortical activity: the Vertex Potential (VP), which is likely related to the optimisation of rapid behavioral responses. In contrast, the functional significance of the brain response elicited by abrupt decreases of sensory input (offsets) is more elusive, and a detailed comparison of onset and offset VPs is lacking. In four experiments conducted on 44 humans, we observed that onset and offset VPs share several phenomenological and functional properties: they (1) have highly similar scalp topographies across time, (2) are both largely comprised of supramodal neural activity, (3) are both highly sensitive to surprise and (4) co-occur with similar modulations of ongoing motor output. These results demonstrate that the onset and offset VPs largely reflect the activity of a common supramodal brain network, likely consequent to the activation of the extralemniscal sensory system which runs in parallel with core sensory pathways. The transient activation of this system has clear implications in optimizing the behavioral responses to surprising environmental changes