Sensation-Targeted Motor Control: Every Spike Counts? Focus on: “Whisker Movements Evoked by Stimulation of Single Motor Neurons in the Facial Nucleus of the Rat”
2008; American Physiological Society; Volume: 99; Issue: 6 Linguagem: Inglês
10.1152/jn.90432.2008
ISSN1522-1598
AutoresErez Simony, Inbar Saraf‐Sinik, David Golomb, Ehud Ahissar,
Tópico(s)Visual perception and processing mechanisms
ResumoEDITORIAL FOCUSSensation-Targeted Motor Control: Every Spike Counts? Focus on: “Whisker Movements Evoked by Stimulation of Single Motor Neurons in the Facial Nucleus of the Rat”Erez Simony, Inbar Saraf-Sinik, David Golomb, and Ehud AhissarErez Simony, Inbar Saraf-Sinik, David Golomb, and Ehud AhissarPublished Online:01 Jun 2008https://doi.org/10.1152/jn.90432.2008This is the final version - click for previous versionMoreSectionsPDF (125 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInEmailWeChat Traditionally, sensory processing and motor control have been studied separately, reflecting the belief that sensory and motor streams remain independent until linked via cortical “associative” areas. Although this belief no longer dominates neuroscience, the traditional tendency to continue to study sensory processing and motor control separately is not easily overcome. Only after closely examining operation of sensory organs does one realize how important motor control is for sensation. The recent elegant study of Herfst and Brecht reveals how accurate sensation-targeted motor control should be in one such system—the vibrissal system.Even a gross examination of mammalian anatomy reveals that most sensory organs are placed within rich muscular arrays. In fact, seeing, touching, smelling, and tasting are enabled by complex modality-specific muscular systems. Detailed examinations of how sensations are acquired in each of these systems have revealed elaborate patterns of sensation-targeted movements of the relevant sensory organs (Ahissar and Arieli 2001; Ahissar and Knutsen 2008; Engbert 2006; Findlay and Brown 2006; Gamzu and Ahissar 2001; Mainland and Sobel 2006; Martinez-Conde et al. 2004; Murakami 2006). How these movement patterns are controlled to achieve accurate sensation is the subject of on-going research in several laboratories.One important question on this subject concerns the resolution of motor control. The recent study of Herfst and Brecht provides a surprising answer—whisker movements induced by single spikes of some motoneurons (MNs) can be as small as 0.1°, and those of other MNs can be as large as 5° with the mean over the sampled population of MNs being 1.8°. The existence of such large single-spike-evoked movements (“twitches”), which are within the range of whisking amplitudes employed during behavior (Knutsen et al. 2005, 2006; Mitchinson et al. 2007; Towal and Hartmann 2006), implies that when maximal accuracy is required, every spike counts.Herfst and Brecht used a juxtacellular method (Pinault 1996) to evoke single spikes in individual MNs of the lateral facial nucleus (FN) of the anesthetized rat and high-resolution video to measure the resulting whisker movements. They found that motor control in this system is based on a labeled-line coding scheme: each neuron is constantly linked to a specific set of movements, and each spike (if isolated in time) constantly, and reliably, evokes a well-defined twitch. The reliability with which each single-spike produced a twitch was extremely high. In their sample, the failure rate was zero, there were no false-alarms (i.e., twitches without spikes), and twitch-to-twitch amplitude variations were low.Effects of single spikes on muscle force have been studied extensively (Burke 1967; van Eijden and Turkawski 2001), and the time course of single muscle twitches has been repeatedly described in textbooks. However, as far as we know, whether motor systems control the occurrence of single MN spikes has not yet been critically considered. The findings of Herfst and Brecht allow a quantitative assessment of this question based on their measurements of the resulting whisker angles. Measurements of whisker angles, rather than muscle forces, allow direct comparison of motor and sensory resolutions. Such a comparison is crucial for understanding vibrissal motor control, the target of which is sensory acquisition, and which allows accurate sensation via gentle active palpation (Carvell and Simons 1995; Knutsen et al. 2006; Mehta et al. 2007; Ritt et al. 2008; Sachdev et al. 2001; von Heimendahl et al. 2007). In fact, using active gentle palpation, rats can detect left versus right horizontal offsets as small as 1° (Knutsen et al. 2006).How detailed should motor control be to allow 1° sensory resolution? In an open-loop system, such a question would be meaningless—sensory resolution would only depend on the sensitivity of sensory receptors per a priori determined motor trajectories. However, active touch is a closed-loop process. During active palpation, rats change whisking amplitudes, velocities, and durations from cycle to cycle until an accurate perception is achieved (Knutsen et al. 2005, 2006; Mehta et al. 2007) or optimal impingement is obtained (Mitchinson et al. 2007). In such a closed-loop system, we posit, motor resolution should be at least of the same order as sensory resolution to allow the system to converge on accurate solutions. Indeed careful tracking of whisker movements reveals whisker movements of a few degrees (at the limit of current tracking noise limitations) that appear to be controlled by the rat during localization (Knutsen et al. 2005, 2006; Mehta et al. 2007) and exploration tasks (Mitchinson et al. 2007; Towal and Hartmann 2006). Given the large range of protracting twitch amplitudes measured by Herfst and Brecht (0.12–5.6°), the identity of activated motor units is crucial. Moreover, for most vibrissal MNs, the occurrence of every single spike is crucial. Thus the vibrissal system must control the firing of these MNs on a unit-by-unit and spike-by-spike basis. An uncontrolled spike might move a whisker beyond the spatial interval to be sensed, inducing a significant sensory error.Much of our knowledge about the neural basis of motor activation comes from research on skeletal muscles that focuses on force generation in the context of movement-targeted motor control. From these studies, the concept of “motor unit” was defined as the set of tens to hundreds muscle fibers innervated by a single MN. Several motor-unit types, which differ in the muscle fibers they contain, have been identified: slow (type 1), fast fatigue-resistant (type 2A), and fast fatigable (types 2B and 2D). During muscle contraction, motor units are often recruited according to the size principle: smaller before larger (Henneman 1985).Utilization of the size principle in the FN might eliminate the need to maintain a detailed unit-by-unit control along vibrissal sensory-motor loops. According to one implementation of the size principle, a given input can only activate MNs the size of which is smaller than a given threshold. Thus, if all MNs affiliated with a given whisker receive the same input, the resulting movement will be proportional to this input. As the input intensity increases, more (and larger) MNs will be recruited. With such mechanism, unit-by-unit selection could be implemented, at least to some extent, by the size principle, and movement amplitude (or velocity) could be controlled by the intensity of the common input to FN sub-populations.Because muscle fibers have only one trick—contraction—additional components in the system have to be recruited to return a joint or a whisker to its resting position. In most skeletal muscle systems, movement reversal is achieved via antagonistic arrangement of muscles. In contrast, in the vibrissal system, movement reversal is achieved by a balance between intrinsic muscles (1 per whisker), extrinsic muscles (4 per whisker-pad), and elastic forces of the tissue (Dorfl 1982). Recently a remarkable understanding of the intricate control of whisking via the set of intrinsic and extrinsic (3 of the 4) muscles of the whisker pad has been obtained (Hill et al. 2008). Hill et al. found that during typical bouts of whisking in air, one of the extrinsic muscles (the m. nasalis) pulls the entire pad forward at the beginning of each whisking cycle, the intrinsic muscles of all whiskers join with a short phase lag and pull the whiskers to their maximal protracted position, and the two caudal extrinsic muscles (the m. nasolabialis and m. maxillolabialis), join with additional phase lag to initiate whisker retraction. The muscular interplay that occurs during active touch, when whiskers palpate an object, is not yet known. From Herfst and Brecht's study, it is clear that fine position control is possible in both the protraction and retraction directions. However, the high proportion of pad muscles dedicated to protraction, the high proportion of FN neurons “labeled for” protraction (Herfst and Brecht 2008; Klein and Rhoades 1985), and the tenability of protraction to environmental changes (Carvell and Simons 1990), indicate that protraction is the direction most finely controlled by the vibrissal system. This is consistent with the vibrissal system being primarily controlled for sensation because most encounters with external objects are expected during whisker protraction.The intrinsic whisker musculature is thus the primary target of motor control in the vibrissal system. Unlike skeletal muscles, intrinsic whisker muscles consist almost exclusively of fast contractible, fast fatigable muscle fibers (Jin et al. 2004). So far, the intrinsic muscles have not been shown to contain muscle spindles, and because they are not linked to bony elements, they are not associated with any other proprioceptors. Thus the control system of these intrinsic muscles differs from that of most skeletal muscles by not having direct proprioceptive feedback to monitor muscle state. Instead proprioceptive information is sensed by mechanoreceptors in the whisker follicle and fed back indirectly via “whisking” sensory neurons (Szwed et al. 2003). Thus the shortest control loop in the vibrissal system contains at least three synapses (Nguyen and Kleinfeld 2005), compared with two in most skeletal systems. How this difference affects control efficiency is another open question.The range of twitch profiles characterized by Herfst and Brecht may serve as a motor alphabet of vibrissal control. The syntax that is used to compose elements of this alphabet into continuous whisking movements is not yet known. However, Herfst and Brecht's limited sample shows that this syntax is not linear in the regime of small amplitudes. In agreement with well-documented studies of contraction profiles in skeletal muscles, Herfst and Brecht show that two consequent spikes do not necessarily evoke the sum of their individual movement amplitudes and that the evoked movement depends on the inter-spike interval (Herfst and Brecht's Fig. 6, C and E) (Ding et al. 2000). Understanding of temporal summation, as well as characterization of spatial summation across different motor units, will require further experiments. With large amplitudes, it is also clear that summation of twitches cannot be linear because as a whisker approaches its maximal protraction angle, the contribution of a given muscle contraction gradually decreases due to increased tissue resistance (Hill et al. 2008) and inability of muscles to contract below a certain length.Unlike skeletal muscles, intrinsic vibrissal muscles are not attached to bones. Rather each such muscle is coupled to two adjacent whisker follicles such that its contraction protracts the whiskers attached to both of them (Fig. 1) (Dorfl 1982). So is the target of a single vibrissal motor unit the anterior, posterior, or both whiskers attached to it? Herfst and Brecht show that all three are possible. Assuming that most of the protraction twitches are evoked via intrinsic muscles and not via the m. nasalis extrinsic muscle, the wide range of anterior/posterior amplitude ratios (0.15–4.6) indicates that motor units can primarily affect either the posterior or anterior whisker, depending, possibly, on their position along the intrinsic muscle (Fig. 1). However, the possibility that single whisker twitches are mediated via extrinsic motor units should not be ruled out. In fact, examples of single-whisker retractions strongly suggest that the specific location of an extrinsic motor unit is crucial in determining how many whiskers it can affect.The vibrissal system is not the only system in which single-spike control might be important. For example, in the visual system sensory and motor resolutions also appear to be similar (Ahissar and Arieli 2001), and to be in the order of eye rotations induced by individual MN spikes (Goldberg et al. 1998). Similarly, motor-sensory loops that control gentle grasping (Flanagan et al. 1999; McDonnell et al. 2005) might also utilize single-spike resolution.Active sensing is mediated by a complex network of parallel and nested motor-sensory-motor loops (Ahissar and Kleinfeld 2003; Kleinfeld et al. 1999, 2006). Whereas sensory and motor coding in first-order sensory (Szwed et al. 2003, 2006) and motor (Herfst and Brecht 2008) neurons of the vibrissal system is relatively simple, coding in higher centers is more intricate (Ferezou et al. 2006; Haiss and Schwarz 2005; von Heimendahl et al. 2007). Consequently, single-cell stimulations in the motor cortex evoke more complex and less reliable whisker movements (Brecht et al. 2004). Nevertheless the fact that short bursts of single cells in the motor cortex can eventually result in a well-defined whisker movement [and can bias rat behavior when induced in the sensory cortex (Houweling and Brecht 2008)] suggests that the contribution of single spikes, anywhere in the vibrissal system should not be underrated. FIG. 1.Schematic biomechanical diagram of one row of whiskers. The row includes five follicles (named β, B1–B4), muscles, and visco-elastic elements (springs and dampers) representing the elasticity of the mystacial pad. The whiskers can be moved forward by contraction of the rostral extrinsic muscle m. nasalis (N), rotated forward by contraction of the intrinsic muscles (grey ellipses) and retracted by contraction of the caudal extrinsic muscles m. nasolabialis and m. maxillolabialis (R). Two axons of the motor nerve (VII) are illustrated to demonstrate potential position specificity of motor units (Adapted from Hill et al. 2008 and Dorfl 1985).Download figureDownload PowerPointREFERENCESAhissar and Arieli 2001 Ahissar E, Arieli A. Figuring space by time. Neuron 32: 185–201, 2001.Crossref | PubMed | ISI | Google ScholarAhissar and Kleinfeld 2003 Ahissar E, Kleinfeld D. Closed-loop neuronal computations: focus on vibrissa somatosensation in rat. Cereb Cortex 13: 53–62, 2003.Crossref | PubMed | ISI | Google ScholarAhissar and Knutsen 2004 Ahissar E, Knutsen PM. Object localization with whiskers. Biol Cybern 98: 449–458, 2008.Crossref | PubMed | ISI | Google ScholarBrecht et al. 2004 Brecht M, Schneider M, Sakmann B, Margrie TW. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427: 704–710, 2004.Crossref | PubMed | ISI | Google ScholarBurke 1967 Burke RE. Motor unit types of cat triceps surae muscle. J Physiol 193: 141–160, 1967.Crossref | PubMed | ISI | Google ScholarCarvell and Simons 1990 Carvell GE, Simons DJ. Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10: 2638–2648, 1990.Crossref | PubMed | ISI | Google ScholarCarvell and Simons 1995 Carvell GE, Simons DJ. Task- and subject-related differences in sensorimotor behavior during active touch. Somatosens Mot Res 12: 1–9, 1995.Crossref | PubMed | ISI | Google ScholarDing et al. 2000 Ding J, Wexler AS, Binder-Macleod SA. Development of a mathematical model that predicts optimal muscle activation patterns by using brief trains. J Appl Physiol 88: 917–925, 2000.Link | ISI | Google ScholarDorfl 1982 Dorfl J. The musculature of the mystacial vibrissae of the white mouse. J Anat 135: 147–154, 1982.PubMed | ISI | Google ScholarEngbert 2006 Engbert R. Microsaccades: a microcosm for research on oculomotor control, attention, and visual perception. Prog Brain Res 154: 177–192, 2006.Crossref | PubMed | ISI | Google ScholarFerezou et al. 2006 Ferezou I, Bolea S, Petersen CC. Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50: 617–629, 2006.Crossref | PubMed | ISI | Google ScholarFindlay and Brown 2006 Findlay JM, Brown V. Eye scanning of multi-element displays. II. Saccade planning. Vision Res 46: 216–227, 2006.Crossref | PubMed | ISI | Google ScholarFlanagan et al. 1999 Flanagan JR, Burstedt MK, Johansson RS. Control of fingertip forces in multidigit manipulation. J Neurophysiol 81: 1706–1717, 1999.Link | ISI | Google ScholarGamzu and Ahissar 2001 Gamzu E, Ahissar E. Importance of temporal cues for tactile spatial frequency discrimination. J Neurosci 21: 7416–7427, 2001.Crossref | PubMed | ISI | Google ScholarGoldberg et al. 1998 Goldberg SJ, Meredith MA, Shall MS. Extraocular motor unit and whole muscle responses in the lateral rectus muscle of the squirrel monkey. J Neurosci 18: 10629–10639, 1998.Crossref | PubMed | ISI | Google ScholarHaiss and Schwarz 2005 Haiss F, Schwarz C. Spatial segregation of different modes of movement control in the whisker representation of rat primary motor cortex. J Neurosci 25: 1579–1587, 2005.Crossref | PubMed | ISI | Google ScholarHenneman 1985 Henneman E. The size-principle: a deterministic output emerges from a set of probabilistic connections. J Exp Biol 115: 105–112, 1985.Crossref | PubMed | ISI | Google ScholarHerfst and Brecht 2008 Herfst LJ, Brecht M. Whisker movements evoked by stimulation of single motor neurons in the facial nucleus of the rat. J Neurophysiol doi: 10.1152/jn.01014.2007.Link | ISI | Google ScholarHill et al. 2008 Hill DN, Bermejo R, Zeigler HP, Kleinfeld D. Biomechanics of the vibrissa motor plant in rat: rhythmic whisking consists of triphasicf neuromuscular activity. J Neurosci 28: 3438–3455, 2008.Crossref | PubMed | ISI | Google ScholarHouweling and Brecht 2008 Houweling AR, Brecht M. Behavioural report of single neuron stimulation in somatosensory cortex. Nature 451: 65–68, 2008.Crossref | PubMed | ISI | Google ScholarJin et al. 2004 Jin TE, Witzemann V, Brecht M. Fiber types of the intrinsic whisker muscle and whisking behavior. J Neurosci 24: 3386–3393, 2004.Crossref | PubMed | ISI | Google ScholarKlein and Rhoades 1985 Klein BG, Rhoades RW. Representation of whisker follicle intrinsic musculature in the facial motor nucleus of the rat. J Comp Neurol 232: 55–69, 1985.Crossref | PubMed | ISI | Google ScholarKleinfeld et al. 2006 Kleinfeld D, Ahissar E, Diamond ME. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr Opin Neurobiol 16: 435–444, 2006.Crossref | PubMed | ISI | Google ScholarKleinfeld et al. 1999 Kleinfeld D, Berg RW, O'Connor SM. Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosens Mot Res 16: 69–88, 1999.Crossref | PubMed | ISI | Google ScholarKnutsen et al. 2005 Knutsen PM, Derdikman D, Ahissar E. Tracking whisker and head movements in unrestrained behaving rodents. J Neurophysiol 93: 2294–2301, 2005.Link | ISI | Google ScholarKnutsen et al. 2006 Knutsen PM, Pietr M, Ahissar E. Haptic object localization in the vibrissal system: behavior and performance. J Neurosci 26: 8451–8464, 2006.Crossref | PubMed | ISI | Google ScholarMainland and Sobel 2006 Mainland J, Sobel N. The sniff is part of the olfactory percept. Chem Senses 31: 181–196, 2006.Crossref | PubMed | ISI | Google ScholarMartinez-Conde et al. 2004 Martinez-Conde S, Macknik SL, Hubel DH. The role of fixational eye movements in visual perception. Nat Rev Neurosci 5: 229–240, 2004.Crossref | PubMed | ISI | Google ScholarMcDonnell et al. 2005 McDonnell MN, Ridding MC, Flavel SC, Miles TS. Effect of human grip strategy on force control in precision tasks. Exp Brain Res 161: 368–373, 2005.Crossref | PubMed | ISI | Google ScholarMehta et al. 2007 Mehta SB, Whitmer D, Figueroa R, Williams BA, Kleinfeld D. Active spatial perception in the vibrissa scanning sensorimotor system. PLoS Biol 5: e15, 2007.Crossref | PubMed | ISI | Google ScholarMitchinson et al. 2007 Mitchinson B, Martin CJ, Grant RA, Prescott TJ. Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact. Proc Biol Sci 274: 1035–1041, 2007.Crossref | PubMed | ISI | Google ScholarMurakami 2006 Murakami I. Fixational eye movements and motion perception. Prog Brain Res 154: 193–209, 2006.Crossref | PubMed | ISI | Google ScholarNguyen and Kleinfeld 2005 Nguyen QT, Kleinfeld D. Positive feedback in a brain stem tactile sensorimotor loop. Neuron 45: 447–457, 2005.Crossref | PubMed | ISI | Google ScholarPinault 1996 Pinault D. A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J Neurosci Methods 65: 113–136, 1996.Crossref | PubMed | ISI | Google ScholarRitt et al. 2008 Ritt JT, Andermann ML, Moore CI. Embodied information processing: vibrissa mechanics and texture features shape micromotions in actively sensing rats. Neuron 57: 599–613, 2008.Crossref | PubMed | ISI | Google ScholarSachdev et al. 2001 Sachdev RNS, Sellien H, Ebner F. Temporal organization of multi-whisker contact in rats. Somat Motor Res 18: 91–100, 2001.Crossref | PubMed | ISI | Google ScholarSzwed et al. 2003 Szwed M, Bagdasarian K, Ahissar E. Encoding of vibrissal active touch. Neuron 40: 621–630, 2003.Crossref | PubMed | ISI | Google ScholarSzwed et al. 2006 Szwed M, Bagdasarian K, Blumenfeld B, Barak O, Derdikman D, Ahissar E. Responses of trigeminal ganglion neurons to the radial distance of contact during active vibrissal touch. J Neurophysiol 95: 791–802, 2006.Link | ISI | Google ScholarTowal and Hartmann 2006 Towal RB, Hartmann MJ. Right-left asymmetries in the whisking behavior of rats anticipate head movements. J Neurosci 26: 8838–8846, 2006.Crossref | PubMed | ISI | Google Scholarvan Eijden and Turkawski 2001 van Eijden TM, Turkawski SJ. Morphology and physiology of masticatory muscle motor units. Crit Rev Oral Biol Med 12: 76–91, 2001.Crossref | PubMed | Google Scholarvon Heimendahl et al. 2007 von Heimendahl M, Itskov PM, Arabzadeh E, Diamond ME. Neuronal activity in rat barrel cortex underlying texture discrimination. PLoS Biol e305, 2007.Google ScholarAUTHOR NOTESAddress for reprint requests and other correspondence: E. Ahissar, Department of Neurobiology, The Weizmann Institute of Science, Rehovot 76100, Israel (E-mail: [email protected]) Download PDF Previous Back to Top Next FiguresReferencesRelatedInformationCited ByPerception as a closed-loop convergence process9 May 2016 | eLife, Vol. 5And motion changes it all1 December 2008 | Nature Neuroscience, Vol. 11, No. 12 More from this issue > Volume 99Issue 6June 2008Pages 2757-2759 Copyright & PermissionsCopyright © 2008 by the American Physiological Societyhttps://doi.org/10.1152/jn.90432.2008PubMed18400953History Published online 1 June 2008 Published in print 1 June 2008 Metrics
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