The implications of a situated, embodied and dynamic perspective on cognition for modern neuroscience

Coherent and complex behaviour emerges from the mutual interaction of brain, body and environment across multiple time-scales and not from within the brain alone [1, 2]. Consequently, the only genuine approach to understanding cognition is from a situated (interacting with an environment), embodied (having a body) and dynamic (spread through time), or SED, perspective [3, 4, 5]. These assertions have a long pedigree within philosophy [6, 7] and are beginning to have a major impact on the ideas and even the language of the cognitive sciences [8, 9]. Furthermore, the field of SED intelligence has grown immensely in the last decade and a fundamental conceptual framework described in terms of information and dynamical system theory has begun to take shape [10]. While the importance of extended dynamic processes and the body/environment context of an organism is at least implicitly understood in the neurosciences it has rarely been explicitly addressed outside of specific invertebrate systems, see [11] for a good review. A major goal of my work is to articulate the implications of this perspective for the neurosciences more generally.

To do this I start from a systems level rather than a system specific perspective more common in traditional neuroethology (the study of the neural basis of behaviour) [11, 12]. However, I subsequently attempt to ground all ideas within specific systems, draw quantitative correspondence between macroscopic dynamics and microscopic detail and identity the possible functional utility of the core ideas for neural computation. I provide two concrete examples of this approach below.

Cognition arises from the interaction of brain, body and environment

The dynamic interaction of brain, body and environment serves as a powerful resource for coherent behaviour in addition to the brain [34, 17, 5]. Indeed, it has been claimed that coherent behaviour is not apriori dependent on the existence of internal dynamics within the brain at all. For example early work in behaviour based robotics by Rodney Brooks demonstrated that the integration of information from different sensory modalities can arise from the interaction of an agent with its environment indirectly [3]. More recent work has shown that behaviours that require memory can arise even when the nervous system lacks any explicit mechanism for state retention (for example a feed-forward system) given a rich enough environment [35]. More specifically we have shown that categorically discrete behaviours can arise even in the absence of corresponding discrete dynamical structures within the nervous system [17].

Studies in invertebrates have made considerable progress grounding these ideas in biological systems [36, 37, 38] but they have had very little impact on vertebrate dominated mainstream neuroscience. However one area of vertebrate neuroscience where the the interaction of brain and body environment is foregrounded is active perception [39]. Particularly, the whisker system of mice and rats has well circumscribed sensory/motor loops involving early sensory relays, thalamus and cortical regions [40]. The onset of whisking, and hence interactions between brain and body, is concomitant with qualitative changes in neural dynamics which constitute a so called brain state change [41]. All investigations of these phenomena so far have focussed on looking for internal triggers for these changes [42, 43]. However, we have argued that brain state changes are mediated by the onset of brain/body environment interactions (i.e. whisking) themselves [44, 45, 46]. This could comprise the first concrete example where the brain/body feedback is fundamental to the description of the neuronal phenomenon itself in a vertebrate system. We are currently collaborating with Fuji lab, RIKEN BSI (Brain Science Institute) utilising electro-cortiography (ECoG) to validate this theory by examining the impact of brain/machine/brain (BMBI) induced correlations on cortical brain dynamics.

Future Prospects

Recent technical innovations promise to give SED ideas renewed relevance for mainstream vertebrate neuroscience. The increasing prevalence of techniques that measure from neural populations with high temporal accuracy (multielectrode and optogenetic techniques) is bringing the neural dynamics of categorisation into sharp relief in other areas other than the olfactory system [47]. It is becoming clear that population responses are not well characterised by steady-state representations or by sets of discrete equilibria [48, 47]. I am extremely excited about extending the dynamical framework we develop in the olfactory systems to other sensory cortices.

The development of Brain Machine Interfaces (BMI), particularly for the control artificial prosthetics, involves real time decoding of ensembles of cortical neurons [49]. Visual feedback has been shown to be central to the stability of BMI interfaces [50, 51]. Furthermore the desire to provide real-time propriopceptive feedback through BMBI’s has placed dynamics of the sensorimotor loop at the centre of this research [50, 52].

Closed-loop experimental designs are becoming increasingly prominent within the neurosciences. Trackball set-ups allow virtual reality conditions for mice and have been adopted by several high profile labs [53, 54, 55]. Full body de-afferentation and environment simulation in the larval zebrafish promises whole brain measurement in the behaving animals [56] . Real-time feedback studies in songbird provide a partial but temporally precise insight into feedback dynamics [57]. Consequently, in vivo electrophysiology and optogenetics of behaving animals is quickly becoming an achievable gold standard in neuroscience. Preliminary studies already suggest that these methods challenge our pre-existing conceptions of neural function. Many neural phenomena have been shown to be contingent on the presence or absence of environmental feedback [57, 54]. We are now just beginning to bring to bear the theoretical framework we have developed for active perception to account for these differences. In my opinion the ideas developed by taking an SED perspective on cognition are on the ascendancy in modern neuroscience.


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