Title: Neuronal Basis for Object Location in the Vibrissa Scanning Sensorimotor System
Abstract: An essential issue in perception is how the location of an object is estimated from tactile signals in the context of self-generated changes in sensor configuration. Here, we review the pathways and dynamics of neuronal signals that encode touch in the rodent vibrissa sensorimotor system. Rodents rhythmically scan an array of long, facial hairs across a region of interest. Behavioral evidence shows that these animals maintain knowledge of the azimuthal position of their vibrissae. Electrophysiological measurements have identified a reafferent signal of the azimuth that is coded in normalized coordinates, broadcast throughout primary sensory cortex and provides strong modulation of signals of vibrissa contact. Efferent signals in motor cortex report the range of the scan. Collectively, these signals allow the rodent to form a percept of object location. An essential issue in perception is how the location of an object is estimated from tactile signals in the context of self-generated changes in sensor configuration. Here, we review the pathways and dynamics of neuronal signals that encode touch in the rodent vibrissa sensorimotor system. Rodents rhythmically scan an array of long, facial hairs across a region of interest. Behavioral evidence shows that these animals maintain knowledge of the azimuthal position of their vibrissae. Electrophysiological measurements have identified a reafferent signal of the azimuth that is coded in normalized coordinates, broadcast throughout primary sensory cortex and provides strong modulation of signals of vibrissa contact. Efferent signals in motor cortex report the range of the scan. Collectively, these signals allow the rodent to form a percept of object location. Animals must determine the position of objects and other animals in their environment, far and near, as they navigate and search. 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., 2006Kleinfeld D. Ahissar E. Diamond M.E. Active sensation: insights from the rodent vibrissa sensorimotor system.Curr. Opin. Neurobiol. 2006; 16: 435-444Crossref PubMed Scopus (151) Google Scholar, König and Luksch, 1998König P. Luksch H. Active sensing—closing multiple loops.Z. Naturforsch., C, J. Biosci. 1998; 53: 542-549PubMed Google Scholar, Nelson and MacIver, 2006Nelson M.E. MacIver M.A. Sensory acquisition in active sensing systems.J. Comp. Physiol. Sensory Neural. Behav. Physiol. 2006; 192: 573-586Crossref PubMed Scopus (59) Google Scholar). Even the sense of smell involves detection at a distance as odorants are carried along plumes (Wachowiak, 2011Wachowiak M. All in a sniff: olfaction as a model for active sensing.Neuron. 2011; 71: 962-973Abstract Full Text Full Text PDF PubMed Scopus (29) Google Scholar). In all of these cases, animals can use stereopsis or an analogous variant to gauge the distance of objects to their body as well as their relative orientation. A different ethological problem arises when objects or conspecifics are close by, so that stereopsis is no longer effective. The perception of nearby objects is particularly acute with animals that track or borrow. Here, long pliable hairs, or in the case of insects long antennae, are used to probe the near environment. In many cases, the hairs or antennae are mobile so that a bilateral scan allows the animal to probe the entire region about its head and provides a shell of detection to keep the animals head from directly touching objects. The computational problem poised by the use of moving sensors in general, and long facial hairs in particular to sense nearby objects, is that sensation and motor control are intertwined. The perception of where an object is relative to the face of the animal requires that the contact of the hairs must be assessed relative to their changing position in space. The problem of object localization with moving sensors was first discussed by Descartes, 1637Descartes, R. (1637). Discourse on Methods, Optics, Geometry, and Meteorology, P.J. Olscamp (trans.) (Indianapolis, IN: Hackett Publsihing Compant).Google Scholar. With reference to a drawing of a blind man with walking sticks (Figure 1A ), he notes "…when the blind man… turns his hand A towards E, or again his hand C towards E, the nerves embedded in that hand cause a certain change in his brain, and through this change his soul can know not only the place A or C but also all the other places located on the straight line AE or CE; in this way his soul can turn its attention to the objects B and D, and determine the places they occupy without in any way knowing or thinking of those which his hands occupy. Similarly, when our eye or head is turned in some direction, our soul is informed of this by the change in the brain which is caused by the nerves embedded in the muscles used for these movements." Steps toward the solution of this neuronal computational problem are the focus of this review. The rat vibrissa system, with its tactile hairs and their associated neuronal architecture, provides a prototype sensorimotor system (Figure 1B). For nearly a century, researchers have compiled behavioral evidence that the vibrissae are both sensors and effectors in a complex sensory system that is able to locate and identify objects (Brecht et al., 1997Brecht M. Preilowski B. Merzenich M.M. Functional architecture of the mystacial vibrissae.Behav. Brain Res. 1997; 84: 81-97Crossref PubMed Scopus (237) Google Scholar, Gustafson and Felbain-Keramidas, 1977Gustafson J.W. Felbain-Keramidas S.L. Behavioral and neural approaches to the function of the mystacial vibrissae.Psychol. Bull. 1977; 84: 477-488Crossref PubMed Scopus (23) Google Scholar). The pioneering work of Vincent, 1912Vincent S.B. The function of the vibrissae in the behavior of the white rat.Behavior Monographs. 1912; 1: 7-81Google Scholar indicated that rats use this system for detection of surfaces during navigation. More recent studies have shown that the vibrissae provide information about object distance (Shuler et al., 2001Shuler M.G. Krupa D.J. 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A clean paradigm is to test if an animal with a single vibrissa can determine the relative position of a pin within the azimuthal sweep of the vibrissa (Figure 2A ). This form of experiment is realized through operant conditioning, in which a rat is trained to maintain a fixed posture and press a lever with a frequency that discriminates between a contact position that is rewarded (S+) versus one that is unreward (S−) (left panel and insert in right panel, Figure 2B). Mehta et al., 2007Mehta S.B. Whitmer D. Figueroa R. Williams B.A. Kleinfeld D. Active spatial perception in the vibrissa scanning sensorimotor system.PLoS Biol. 2007; 5: e15https://doi.org/10.1371/journal.pbio.0050015Crossref PubMed Scopus (50) Google Scholar found that rats can perform this discrimination task within a period of one or two whisks (right panel, Figure 2B). This implies that rats know the azimuthal position of their vibrissae. The results from related work, in which rats were trained to report the relative depth between two pins, suggests that azimuthal acuity is better than 6° (Knutsen et al., 2006Knutsen P.M. Pietr M. Ahissar E. Haptic object localization in the vibrissal system: behavior and performance.J. Neurosci. 2006; 26: 8451-8464Crossref PubMed Scopus (79) Google Scholar). What is the role of cortex in this discrimination task? In particular, while rodents may be trained to discriminate object location, this process could occur at a subcortical level. This question was addressed by O'Connor et al., 2010aO'Connor D.H. Clack N.G. Huber D. Komiyama T. Myers E.W. Svoboda K. Vibrissa-based object localization in head-fixed mice.J. Neurosci. 2010; 30: 1947-1967Crossref PubMed Scopus (67) Google Scholar, who used head-fixed mice trained to discriminate among one of two positions of a pin (left panel, Figure 2C). Mice could perform this task with better than 90% discrimination at an acuity of less than 6°, albeit with a different strategy than found with the case for rats (Knutsen et al., 2006Knutsen P.M. Pietr M. Ahissar E. Haptic object localization in the vibrissal system: behavior and performance.J. Neurosci. 2006; 26: 8451-8464Crossref PubMed Scopus (79) Google Scholar, Mehta et al., 2007Mehta S.B. Whitmer D. Figueroa R. Williams B.A. Kleinfeld D. Active spatial perception in the vibrissa scanning sensorimotor system.PLoS Biol. 2007; 5: e15https://doi.org/10.1371/journal.pbio.0050015Crossref PubMed Scopus (50) Google Scholar). Here, rather than sweep their vibrissae, the animals tended to hold or slowly move their vibrissae near the site that one of the two pins was lowered. This difference aside, the ability to discriminate azimuthal location was lost when vibrissa primary sensory (vS1) cortex was shut down through an infusion of the GABAA agonist muscimol, and recovered upon wash out (right panel, Figure 2C). A potential caveat in this experiment is that inactivation of vS1 cortex can affect the ability of a rodent to whisk (Harvey et al., 2001Harvey M.A. Bermejo R. Zeigler H.P. Discriminative whisking in the head-fixed rat: optoelectronic monitoring during tactile detection and discrimination tasks.Somatosens. Mot. Res. 2001; 18: 211-222Crossref PubMed Scopus (86) Google Scholar, Matyas et al., 2010Matyas F. Sreenivasan V. Marbach F. Wacongne C. Barsy B. Mateo C. Aronoff R. Petersen C.C. Motor control by sensory cortex.Science. 2010; 330: 1240-1243Crossref PubMed Scopus (73) Google Scholar), so the transient loss in discrimination could reflect a motor rather than sensory defecit. In toto, behavioral data implies that the rodent vibrissa system is an valuable model to study the merge of sensor contact and position, and that vS1 cortex is likely to play a necessary role in computing the relative angle of touch. What are the neural pathways that support signals of vibrissa touch and position? We review the anatomy of the vibrissa sensorimotor system so that physiological measurements can be placed in the context of high level circuitry (Figure 3). The basic layout of the sensorimotor system is one of nested loops (Kleinfeld et al., 1999Kleinfeld D. Berg R.W. O'Connor S.M. Anatomical loops and their electrical dynamics in relation to whisking by rat.Somatosens. Mot. Res. 1999; 16: 69-88Crossref PubMed Scopus (119) Google Scholar). The follicles, which are both sensors through their support of vibrissae and effectors through their muscular drive, and the mystacial pad that supports the follicles form the common node in these loops. Afferent input is generated by shear or compression of mechanosensors in the follicles (Kim et al., 2011Kim J.N. Koh K.S. Lee E. Park S.C. Song W.C. The morphology of the rat vibrissal follicle-sinus complex revealed by three-dimensional computer-aided reconstruction.Cells Tissues Organs. 2011; 193: 207-214PubMed Google Scholar, Rice, 1993Rice F.L. Structure, vascularization, and innervation of the mystacial pad of the rat as revealed by the lectin Griffonia simplicifolia.J. Comp. Neurol. 1993; 337: 386-399Crossref PubMed Scopus (23) Google Scholar). The afferent signal propagates through primary sensory cells in the trigeminal ganglion, whose axons form the infraorbital branch of the trigeminal nerve. These cells make synaptic contacts onto neurons that lie within different nuclei of the trigeminus, all arranged in parallel. Of note is the one-to-one map of the input from the follicles onto the nucleus principalis (PrV) and the caudal division of the spinal nucleus interpolaris (SpVIc) (left column, Figure 3). A projection, but not one-to-one mapping, also occurs to the rostral division of nucleus interpolaris (SpVIr). Two feedback loops in the brainstem condition the incoming sensory input. First, cells in nucleus SpVIc, which respond to an individual vibrissa, form inhibitory synapses onto neurons in nucleus PrV (red arrow in middle row, Figure 3). This feedback acts to spatially and temporally sharpen the response in a "center-surround" manner (Bellavance et al., 2010Bellavance M.A. Demers M. Deschênes M. Feedforward inhibition determines the angular tuning of vibrissal responses in the principal trigeminal nucleus.J. Neurosci. 2010; 30: 1057-1063Crossref PubMed Scopus (10) Google Scholar, Furuta et al., 2008Furuta T. Timofeeva E. Nakamura K. Okamoto-Furuta K. Togo M. Kaneko T. Deschênes M. Inhibitory gating of vibrissal inputs in the brainstem.J. Neurosci. 2008; 28: 1789-1797Crossref PubMed Scopus (26) Google Scholar). A second feedback pathway involves projections from the SpVI and SpVC trigeminal nuclei to the facial motoneurons, which independently drive motion of the follicle and that of the mystacial pad (Hill et al., 2008Hill D.N. Bermejo R. Zeigler H.P. Kleinfeld D. Biomechanics of the vibrissa motor plant in rat: rhythmic whisking consists of triphasic neuromuscular activity.J. Neurosci. 2008; 28: 3438-3455Crossref PubMed Scopus (51) Google Scholar, Klein and Rhoades, 1985Klein B.G. Rhoades R.W. Representation of whisker follicle intrinsic musculature in the facial motor nucleus of the rat.J. Comp. Neurol. 1985; 232: 55-69Crossref PubMed Google Scholar). This in turn leads to activation of the mystacial muscles and a forward thrust of the vibrissae upon contact (Nguyen and Kleinfeld, 2005Nguyen Q.-T. Kleinfeld D. Positive feedback in a brainstem tactile sensorimotor loop.Neuron. 2005; 45: 447-457Abstract Full Text Full Text PDF PubMed Scopus (54) Google Scholar, Sachdev et al., 2003Sachdev R.N.S. Berg R.W. Champney G. Kleinfeld D. Ebner F.F. Unilateral vibrissa contact: changes in amplitude but not timing of rhythmic whisking.Somatosens. Mot. Res. 2003; 20: 163-169Crossref PubMed Scopus (31) Google Scholar). In principle, the latter feedback provides the animal with a means to distinguish between spikes in the trigeminus that are unrelated to contact, for which the thrust would push the vibrissae forward without the generation of additional spikes, and a true touch event, where the thrust enhances contact and can provide additional spikes. The single projection from the trigeminal nucleus to the facial nucleus is paralleled by multiple polysynaptic pathways at the level of the brainstem and midbrain, e.g., the superior colliculus, and by pathways that extend through the forebrain (Kleinfeld et al., 1999Kleinfeld D. Berg R.W. O'Connor S.M. Anatomical loops and their electrical dynamics in relation to whisking by rat.Somatosens. Mot. Res. 1999; 16: 69-88Crossref PubMed Scopus (119) Google Scholar; Figure 3); we focus on the latter. There are two major ascending pathways from the trigeminus. Projections from nucleus PrV ascend to the dorsal medial aspect of the ventral posterior medial (VPMdm) nucleus of dorsal thalamus, where they make a triplet of representations (Pierret et al., 2000Pierret T. Lavallée P. Deschênes M. Parallel streams for the relay of vibrissal information through thalamic barreloids.J. Neurosci. 2000; 20: 7455-7462PubMed Google Scholar, Urbain and Deschênes, 2007bUrbain N. Deschênes M. 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The projections cluster into columns, commonly called barrels, that maintain the one-to-one relation with the spatial distribution of the vibrissae (top row, Figure 3). The second set of ascending projections emanate from trigeminal nucleus SpVIr to the medial division of the posterior group (Po) nucleus of dorsal thalamus and involves both direct excitatory input from nucleus SpVIr as well as inhibitory input that comes indirectly via projections to the ventral aspect of the zona incerta (ZIv) (Barthó et al., 2002Barthó P. Freund T.F. Acsády L. Selective GABAergic innervation of thalamic nuclei from zona incerta.Eur. J. Neurosci. 2002; 16: 999-1014Crossref PubMed Scopus (86) Google Scholar). The latter input is part of a forebrain loop in which activity in Po thalamus is modulated by projection neurons from vibrissa primary motor (vM1) cortex to ZIv, which inactivates an inhibitory input to Po thalamus (Urbain and Deschênes, 2007aUrbain N. Deschênes M. 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