Dynamics of Active Sensing and perceptual selection

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Sensory processing is often regarded as a passive process in which biological receptors like photoreceptors and mechanoreceptors transduce physical energy into a neural code. Recent findings, however, suggest that: first, most sensory processing is active, and largely determined by motor/attentional sampling routines; second, owing to rhythmicity in the motor routine, as well as to its entrainment of ambient rhythms in sensory regions, sensory inflow tends to be rhythmic; third, attentional manipulation of rhythms in sensory pathways is instrumental to perceptual selection. These observations outline the essentials of an Active Sensing paradigm, and argue for increased emphasis on the study of sensory processes as specific to the dynamic motor/attentional context in which inputs are acquired.

Introduction

‘Active Sensing,’ as a term in robotics, refers to use of a sensor or detector device that requires input energy from a source other than that which is being sensed. Classic examples of Active Sensing in biological systems include echolocation in bats and marine mammals [1] and electrolocation in fish [2]. In contrast, biological sensors like the eyes and finger tips traditionally have been thought of as passive sensors that transduce the energy of the input into a neuronal code. However, closer examination of the manner in which humans and other animals gather data from the environment suggests that overall, it is more of an Active Sensing process. Natural somatosensory exploration, for example, typically involves use of the fingers to feel textures and manipulate objects. Only rarely do we leave the hand still and wait for something to touch it. Similarly in natural viewing, we do not just stare at a spot and wait for things to happen around it, but rather, we actively sample the scene with a systematic pattern of eye movements and fixations [3, 4]. In short, much of the sensory input that enters the brain does so because we actively locate and acquire it using a motor sampling routine. As elaborated in the next section, motor control of sensory inflow has strong implications for the way we must think about sensory processing.

Attention is the neural process by which the brain enhances the representation of task relevant input at the expense of irrelevant input, and it is the essential component of Active Sensing. Attention and motor sampling routines can be dissociated, in that attention can either operate in the absence of any overt motor activity, or can be directed to a location other than that upon which the sensors are aligned, as in covert spatial attention [5]. However, attention in isolation from any motor routine is relatively uncommon in natural Active Sensing.

This paper will explore the concept of Active Sensing as a collaboration of motor and sensory rhythms that is advantageous for information processing. We will review and consider: first, the role of motor activity in Active Sensing, using olfaction and vision as examples; second, the mechanisms by which the rhythms inherent in motor sampling routines may engage corresponding rhythms in olfactory and visual systems, and role of attention in this process; third, the extent to which these concepts generalize to somatosensation and audition. Throughout, we will attempt to make clear the uncertainties and open questions in our perspective.

Section snippets

Rhythm in motor routines used in Active Sensing

Motor output is modulated by motor cortical oscillatory rhythms in the delta (1–3 Hz), theta (5–7 Hz), mu (8–12 Hz), and beta (13–30 Hz) bands [6, 7, 8, 9, 10, 11], and in our view, the motor system's imposition of these rhythms on sensory inflow is a critical factor in Active Sensing. However, the senses vary in the degree to which they explicitly depend on motor routines, and thus also, in their apparent sensitivity to rhythmic motor influences. Olfaction, owing to its utter dependence on the

Neuroelectric oscillations

Neuroelectric oscillations, ubiquitous in the brain of an awake subject at rest [39], reflect a synchronization of cyclical fluctuations in neuronal excitability across populations of neurons, that may be critical to normal sensory processing (reviewed by [40]). Of particular relevance here, we have shown that lower frequency oscillatory rhythms in the range of those observed in sniffing and free viewing can function as instruments of cross modal amplification and attentional selection in

Somatosensation

Given the above considerations and the extensive interconnectivity between primary motor and somatosensory cortices in primates [46], we would expect that motor control of Active Sensing as outlined above would also operate in the somatosensory cortical hand/arm representation. Although there have been studies examining oscillatory activity in the hand representation of primate Area 3b (e.g. [47]), as far as we can determine, this is an open question.

Active Sensing has been examined to some

Conclusions

Passive stimulation paradigms have been a mainstay of basic neuroscience research because they afford simplification and stabilization of complex dynamic phenomena, and they will likely continue to be productive. On the other hand, these paradigms ablate key components of natural experience, particularly the rhythms that are inherent to our motor sampling routines. These drive and/or entrain rhythms in sensory regions that are fundamental tools in normal sensory processing and perceptual

Acknowledgements

The authors’ work is supported by The New York State Office of Mental Health, and by NIH Grants RO1MH061989, RO1MH060358, P50MH086385, R21DC010415, R01DC03906, RO1DC008982, T32MH067763, R21MH084215 and RO1NS037562.

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