Active sensation: Insights from the rodent vibrissa sensorimotor system

“…parts of the corresponding sensory system and/or creating transient gains, which enhance the reader (sensory) system’s ability to process the inputs (Ahissar and Arieli, 2001; Bremmer et al., 2009; Gutierrez et al., 2010; Halpern, 1983; Henson, 1965; Kepecs et al., 2006; Kleinfeld et al., 2006).”

“Rats explore the world largely by whisking tactile objects of interes”

“Action-potential firing and membrane-potential oscillations in the barrel cortex phase locked to the whisking cycle could contribute to encoding the position of whisker object touch (Fee et al., 1997; Szwed et al., 2003; Crochet and Petersen, 2006; Kleinfeld et al., 2006).”

“Sensorimotor Integration in Behaving Mice”

“…representation area of the primary somatosensory cortex (barrel cortex) has favorable properties for relating sensory stimuli, neuronal responses, and behavior in the context of defined anatomical circuits (Diamond et al., 2008; Kleinfeld et al., 2006; O'Connor et al., 2009; Petersen, 2007).”

“Active sensory perception and sensorimotor integration are thus prominent features of this system (Kleinfeld et al., 2006).”

“More recently, based on the whisker motions evoked by electrical stimulation of the FOF, the area has been studied as a whisker motor cortex (Brecht et al., 2004), with particular attention paid to its role in vibrissal active sensing (reviewed in Kleinfeld et al., 2006).”

“The tactile whisker sensorimotor system of the mouse is therefore one attractive model system for beginning a detailed synaptic and circuit-level analysis of the neural mechanisms underlying perception (Kleinfeld et al., 2006; Petersen, 2007; Diamond et al., 2008; O’Connor et al., 2009).”

“These findings support a continuous mutual communication between sensory inflow and motor outflow (Kleinfeld et al., 2006; Lee et al., 2008).”

“When a rat searches its environment, looking for an object to contact and identify, it actively whisks its vibrissae forward and backward at a rate of 5–12 Hz (Carvell and Simons 1990; Kleinfeld et al. 2006; Wi 1964).”

“The whisking motion used to analyze objects is actively controlled by primary motor cortex, and whisking bouts can vary in amplitude and speed (reviewed in [65]).”

“2328" language="eng" relation="no"> How sensory systems encode behaviorally meaningful stimuli during active, natural sensation is a central problem in neuroscience that can be effectively studied in the tactile syste”

“Active sensation has received much attention in the rodent vibrissal system, in which the vibrissae are moved across the input space rhythmically (Kleinfeld et al., 2006; Mehta et al., 2007; Lee et al., 2008).”

“How whiskers read out texture information, and how that information is encoded in the nervous system, are vigorously debated, and have important implications for sensory processing in the whisker system [6,7], which is a major model system for studying”

“This may indicate that this frequency band reflects an optimal time scale for the coordination of the brain activities in the sensory and the motor systems required for active sensing (Kleinfeld et al., 2006; Uchida and Kepecs, 2006; Schroeder et al., 2010).”

“…interest is the possibility that differences in vibrissa properties across the face result in parallel afferent pathways carrying different information (Brecht et al., 1997; Hartmann et al., 2003; Kleinfeld et al., 2006; Mehta and Kleinfeld, 2004; Moore and Andermann, 2005; Neimark et al., 2003).”

“Sensation in the rodent vibrissal system relies on active whisking for interactions with the environment [1,2].”

“In rats, as in humans [1], tactile exploration entails the interplay of motor output and sensory input: Rats palpate objects by sweeping their whiskers in a rhythmic forward–backward cycle [2].”

“A key advance has been the widespread adoption of head-fixation methods, first developed in the primate neurophysiology community (Wurtz, 1969) and then adapted the use in rodents (Dombeck et al., 2007)(see also Kleinfeld and Griesbeck, 2005 and references therein).”

“The follicle is swept rhythmically back and forth by muscles in the mystacial pad to permit the hairs to touch and probe objects that are located close to the head of the animal (Kleinfeld et al., 2006).”

“In rats, as in humans (Gamzu and Ahissar, 2001), tactile object exploration derives from active palpation; rats sweep their whiskers across surfaces in a rhythmic forward– backward cycle to create neuronal representations of the contacted objects (Kleinfeld et al., 2006).”

“In this case, the presence of position-sensitive neurons suggests that the position of the vibrissae at the time of contact could provide context to interpret the contact event [35,36].”

“The bat’s echolocation system, or biological sonar, is an active sensing system, sharing characteristics with other active sensing systems in nature (33): the echolocation system of whales and dolphins (32); the electrolocation system of weakly electric fish (38); the whiskingsomatosensory system of rodents (4); the o…”

“Current Opinion in Neurobiology 2007, 17:408–416 imotor interactions in this system will not be covered here, but these have recently been reviewed [1,2].”

“The vibrissa system in rat provides an ideal model for the investigation of a motor plant that is central to active sensing (Kleinfeld et al., 1999, 2006).”

“The sense of distant objects requires the use of propagating signals, light to see, sound to hear, and for some animals the use of electrical disturbances (Kleinfeld et al., 2006; König and Luksch, 1998; Nelson and MacIver, 2006).”

“Developing statistical approaches that allow rigorous assessment of rare or singular events that make up the long tail of variance in natural behavior remains a key challenge.”

“The higher outstrength from S1 to S2 may suggest that S1 nodes tend to stimulate further responses in other nodes or even in sensory feedback loops, including corticothalamic circuits (Kleinfeld et al., 2006).”

“The rat whisker (vibrissal) system is becoming an increasingly important model to study the role of biomechanics in sensing behaviors (Kleinfeld et al., 2006; Diamond et al., 2008).”

“…to name the state of the sensory system characterized by exploratory whisking as ''active'' and the state of quiet immobility as ''passive'' (Kleinfeld et al., 2006), but we suggest that this nomenclature is misleading in its implication that the nervous system itself becomes passive in the…”

“It has become clear that the thalamus is not a simple relay station of ascending sensory information but is involved in processing of sensory information by integrating input from multiple sources (Kleinfeld et al., 2006; Yu et al., 2006; Urbain and Deschênes, 2007).”

“The spatially tuned responses of the barrel columns have prompted the view that spatial coding by the barrel circuitry is used to perceive whichwhiskers are contacted by an external stimulus (Kleinfeld et al. 2006).”

“…perceive the world via active body and sensor movements (Ahissar and Arieli, 2001; Diamond et al., 2008; Findlay and Gilchrist, 2003; Halpern, 1983; Kleinfeld et al., 2006; Konig and Luksch, 1998; Land, 2006; Lederman and Klatzky, 1987; Najemnik and Geisler, 2005; Rucci et al., 2007; Schroeder et…”

“Indeed, rats’ whiskers are used to estimate the shape and location of the objects [Kleinfeld et al., 2006; Diamond et al., 2008].”

“Further, whisking and touch signals are integrated via sensorimotor loops at multiple points along the somatosensory pathway, from brainstem to cortex [34].”

“Our stimulation characteristics were also physiologically relevant, as exploratory whisking in mice is typically 5–15 Hz in 1– 4 s bouts (Kleinfeld et al., 2006).”

“For instance, vibrissal activations and movements in rodents occur at about 10 Hz and give rise to projections to both the pontine nuclei and inferior olive (Kleinfeld et al., 2006) as well as directly from the trigeminal nucleus to the cerebellum (Bower and Woolston, 1983; Morrissette and Bower, 1996).”

“nucleus) and paralemniscal (posterior medial nucleus), somatosensory pathways (Chiaia et al. 1991; Turman et al. 1995; Kim and Ebner 1999; Veinante et al. 2000; Bureau et al. 2006; Kleinfeld et al. 2006; Yu et al. 2006).”

“Indeed, our sensory organs are not passive receptacles for stimulation but are part of an action-perception closed-loop system (Kleinfeld et al. 2006; Schroeder et al. 2010; Ahissar and Assa 2016; Rajkai et al. 2008; Barczak et al. 2019).”

“…oscillation and resonance, together with theta-frequency resonance in granule cells (D’Angelo et al., 2001) may intensify and improve time precision to theta-frequency cortical inputs during certain sensory-motor behaviors, like active whisking (for review see Kleinfeld et al., 2006).”

“One well-known example of a developmentally emergent behavior is exploratory whisking, the rhythmic sweeping movements of vibrissae (or whiskers) that rodents use to detect the texture, shape, and location of objects in their environment (Diamond et al., 2008; Kleinfeld et al., 2006).”

“This behaviour represents a good example of active sensory sampling, where the animal itself modulates when and where it receives sensory input in order to get a better picture of its environmen”

“The rodent whisker system combines relatively simple movements with direct sensory feedback (Vincent, 1913; Welker, 1964; Brecht et al. 2006; Kleinfeld et al. 2006), making it an ideal model system to study sensorimotor integration.”

“Recent progress has been spurred by our increased understanding of natural vibrissal systems and advances in engineering materials, transduction, actuation, and microelectronics.”

“However, the natural stimuli processed by neurons in the whisker system are often generated by active whisking ( Kleinfeld et al., 2006 ).”

“their eyes, whiskers, or hands) so as to extract task-relevant information efficiently (Yarbus, 1967; Kleinfeld et al., 2006; Lederman and Klatzky, 1987).”

“and Kleinfeld, D. (2006) Confluence of position and active touch in rat”

“Such an interleaving of rhythmic movement and information coding has been noted before in hippocampal, somatosensory, and olfactory structures, where theta activity correlates with locomotion, whisking, and respiratory rhythms, respectively (Vanderwolf, 1969; Lisman, 2005; O’Keefe and Burgess, 2005; Kleinfeld et al.,…”

“All 3 cell types had a high probability of receiving direct excitatory M1 input.”

“, 2010), offers the following explanations for the main behaviors of the Golgi cell reported in vivo: pacemaking may underlie the rhythmic Golgi cell discharge in vivo, which, as a result of synaptic inputs, would then become irregular and spread over a broader frequency range (2–25 Hz); resonance could enhance Golgi…”

“Such signals are conveyed by the primary afferent whisking cells (Szwed et al. 2003), and exist in both the somatosensory thalamus (Yu et al. 2006) and barrel cortex (Fee et al. 1997; Brecht et al. 2006; Crochet and Petersen 2006; Derdikman et al. 2006; Kleinfeld et al. 2006 ).”

“It has been suggested that sniffing and whisking allow animals to process continuous real-world sensory stimuli into discrete chunks or cycles (Kleinfeld et al., 2006), with each cycle serving as a temporal frame to synchronize neural activity across multiple brain structures (Nicolelis et al.,…”

“of the eyes, or the vibrissa [19]) and top-down attention to the informative features of the stimulus.”

“Once they encounter an object, they collect additional information about its features, such as its size, shape, and surface texture by palpating it through a “whisking” motion (Grant et al. 2009; Kleinfeld et al. 2006).”

“For example, neurons in the rodent somatosensory cortex exhibit firing rates that scale logarithmically with frequency of tactile stimulation (Kleinfeld et al., 2006).”

“These results are in line with the broader framework of active sensing (Kleinfeld et al., 2006; Collewijn & Kowler, 2008; Bosman et al., 2009; Schroeder & Lakatos, 2009b; Schroeder et al., 2010; Wachowiak, 2011; Kagan & Hafed, 2013; Martinez-Conde, 2013) where the external world is sampled actively through rhythmic se…”

“…theta-frequency oscillation and resonance, together with theta-frequency resonance in granule cells (D’Angelo et al., 2001) may tune granular layer responses toward theta-frequency cortical inputs during certain sensory-motor behaviors, like active whisking (for review see Kleinfeld et al., 2006).”

“Multiple modes of whisker movement occur, including bilateral, 5–12 Hz ‘‘exploratory’’ whisking by macrovibrissae, higher frequency frontal ‘‘foveal’’ whisking by macrovibrissae, and slower translation of both macrovibrissae and microvibrissae across objects by head motion [1 ,5,6].”

“Sensorimotor systems are comprised of nested loops (Kleinfeld et al., 1999, 2006; Bosman et al., 2011).”

“Distinct brain regions make different functional contributions to the encoding of this behavior (Kleinfeld et al., 2006).”

“Rodent whiskers are active tactile detectors that guide sensory and exploratory behavior [1,2].”

“The whisker barrel is a patch of rodent sensorimotor cortex that processes information associated with one contralateral whisker (vibrissa), and is one element of a closely packed somatotopic array of barrels, one per whisker [34,35].”

“The paralemniscal pathway primarily conveys whisking signals, which can be employed to form sensory-motor coordination and positional reference signals during exploration/whisking (Ahissar et al., 2000; Kleinfeld et al., 2006).”

“The vibrissal somatosensory system of rodents is an active sensing system (Ahissar and Arieli, 2001; Kleinfeld et al., 2006); during tactile exploration, rats use rapid whisker movements while sampling the physical environment around them (Vincent, 1912; Welker, 1964; Gustafson and…”

“After the initial description of whisking movements (Welker 1964) improvements in high-speed recording techniques have greatly facilitated the analysis of vibrissal motor control (Carvell and Simons 1990; Kleinfeld et al. 1999, 2006; von Heimendahl et al. 2007).”

“Because whisking is an actively controlled sensory-motor behavior [17,18], its parameters vary from moment to moment.”

“…rhythmic whisker protractions (Ahissar and Knutsen 2008; Brecht 2007; Carvell and Simons 1990; Deschênes et al. 2003; Diamond et al. 2008; Hill et al. 2008; Jadhav and Feldman 2010; Kleinfeld et al. 2006; Knutsen and Ahissar 2009; Mehta et al. 2007; O’Connor et al. 2010; Vincent 1912; Welker 1964).”

“…limited to the primary somatosensory cortex, but involves several other cortical areas, such as the secondary somatosensory cortex, the vibrissal motor cortex, and somatosensory cortices of the opposite hemisphere, as well as subcortical structures (Kleinfeld et al., 2006; Ferezou et al., 2007).”

“This extends our previous findings about the temporal stability of epicranial SEP waveforms (Troncoso et al., 2000) and suggests that the large-scale cortical network activated by whisker stimulation is a fundamental component underlying sensorimotor processing in mice (Kleinfeld et al., 2006).”

“Both rapid and slow modulations can result from top-down control of the whisking circuits and from ex-afferent or re-afferent sensory feedback [1,27].”

“I N T R O D U C T I O N Palpatory vibrissa movements in rodents have emerged as an attractive model for motor control (Brecht et al. 1997; Kleinfeld et al. 2006; Vincent 1912).”

“‘‘Active sensing’’ is a process in which sensory input that enters the brain is actively acquired by motor sampling (Kleinfeld et al., 2006; Schroeder et al., 2010; Hatsopoulos and Suminski, 2011) and is highly conserved across systems and species.”