this gave rise centrally to sensations of muscular activityand movement. Sherrington (355) in his inﬂuential text-bookchapteron“Themuscularsense”rejectedtheseideas,largely based on the observation that in the absence of mo-tor commands, when our limbs lie relaxed, we still knowwhere they are, even if we are not looking at them. Sher-rington stated, “An objection to this hypothesis (sensationof innervation) is that it sunders sharply the sensations of passive from those of active movement, whereas there isstrong ground for believing the two intimately allied.” Sothere were two schools of thought, one claiming that themuscle sense had an entirely central origin, and the otherbelieving that a peripheral signal was principally responsi-ble. Bastian (17), who coined the term
, was theonly one at the time who contemplated a hybrid theory,comprising both central and peripheral components (seealso Ref. 95). He later abandoned this idea in favor of apurely peripheral mechanism [for details, see Jones (204)].Sherrington’s views prevailed, and for the ﬁrst half of the20th century the subject of proprioception was largelyfounded on muscular sensations, although some counterviews were proposed by the psychologist Lashley (222).In his account of the muscle senses, Sherrington passedwithout comment from the role of muscle receptors in “ac-tivemovement”totheircontributiontospinalreﬂexaction.This brushes over the two remarkably different roles of muscle receptors, their contribution to conscious sensationas proprioceptors, and their unconscious, automatic reﬂexaction. This dichotomy of action led Merton (257) to de-clare, “Everyone agrees that the muscle spindles are thereceptorsforthestretchreﬂexandthemechanismsbasedonit, but it is also held at the same time that the muscle spin-dles give information about the length of the muscles to beusedinourconsciousjudgementsoflimbposition.Untiltheunderlying incompatibility of these two notions is felt, onecannot properly appreciate the character of the problemsthat face us in this ﬁeld.” Here it is worth reﬂecting on thestrategy of assigning to one class of receptors such diverseroles and what this means for central integrative processes.In the present review we have limited the meaning of “pro-prioceptor” to a receptor that gives rise to conscious sensa-tions(300).Indoingso,weareawarethatreceptorssuchasmuscle spindles and tendon organs also play importantroles in the unconscious, reﬂex control of movements.When we think about limb position sense, an obvious placeto look for receptors signaling position is in the joint aboutwhich the limb moves. That, indeed, was the prevailingview for much of the 20th century. Kinesthetic sensationswere thought to arise exclusively in the joints. Sherringtonhimself was cautious, “The individual contributions to-ward muscular sense of these different sets of end-organscan only be conjectured” (355). In any case, as single affer-ent recording techniques were introduced, the view arosethat the principal source of kinesthetic information lay inthe joints themselves. The experimental basis for this viewwas provided by Boyd and Roberts (33) and Skoglund(362) [see also Skoglund (363), Mountcastle and Powell(267), and Jones (204)]. Today we know that this is not thecase and that muscle receptors are the principal kinestheticreceptors. In an inﬂuential series of animal studies whichchallenged the view of joint receptors as the principal kin-esthetic sensors, Burgess and colleagues (42, 43) showedthat slowly adapting receptors in the knee joint of the catprovided ambiguous positional information because theyincreased their rate of discharge at both extremes of jointposition. Here there was an interesting twist to the story. Itwasclaimedthatinthecatposteriorarticularnervesupply-ing the knee joint there were afferents which dischargedacross the mid range of knee position (33, 115, 362). Theseafferents changed their discharge rate monotonically withchangesinjointangle,aswouldbeexpectedfromareceptorsignaling joint position. Subsequently, however, these dis-charges were shown to come from muscle spindles in thepopliteus muscle whose afferents had taken an aberrantcourse in the posterior articular nerve (250).The modern view has muscle spindles as the principal pro-prioceptors. Here it is interesting to reﬂect on the tortuouspath taken by progress in the ﬁeld. Early, quite sophisti-cated ideas on a sensation of innervations were replaced bya view that focussed entirely on peripheral receptors. Butthis was still wrong, since the main receptor type was con-sidered to be joint receptors, not muscle receptors. Nowa-days, while we are aware of the importance of peripheralsignals for passive proprioception, we have revived some of the old ideas on a sensation of innervations, to give “out-ﬂow” signals a bigger role, especially in active propriocep-tion, where the generation of peripheral signals is accom-panied by voluntary motor activity.
During limb movement and changes in position, the tissuesaround the relevant joints will be deformed, including skin,muscles,tendons,fascia,jointcapsules,andligaments(e.g.,Refs. 1, 169). All these tissues are innervated by mechani-cally sensitive receptors, and their density varies acrossmuscles and regions of the body (e.g., Ref. 16). The ques-tion arises, which are the principal kinesthetic receptors? Inthis review the view is argued that muscle spindles play themajor role in kinesthesia, with some skin receptors provid-ing additional information. Emerging views suggest thatGolgi tendon organs contribute to proprioception, includ-ing the senses of force and heaviness. Here the evidenceremains indirect, the problem being that it is difﬁcult toactivate a population of tendon organs selectively. The ma-jor features of the muscle spindle and tendon organ aredepicted in
, respectively. Joint receptors
THE PROPRIOCEPTIVE SENSES
onM a y 2 5 ,2 0 1 4 D ownl o a d e d f r om