Abstract

Neuroscience folklore has it that somatotopy in human primary somatosensory cortex (SI) has two significant discontinuities: the hands and face map onto adjacent regions in SI, as do the feet and genitalia. It has been proposed that these conjunctions in SI result from coincident sources of stimulation in the fetal position, where the hands frequently touch the face, and the feet the genitalia. Computer modeling using a Hebbian variant of the self-organizing Kohonen net is consistent with this proposal. However, recent work reveals that the genital representation in SI for cutaneous sensations (as opposed to tumescence) is continuous with that of the lower trunk and thigh. This result, in conjunction with reports of separate face innervation and its earlier onset of sensory function, compared to that of the rest of the body, allows a reappraisal of homuncular organization. It is proposed that the somatosensory homunculus comprises two distinct somatotopic regions: the face representation and that of the rest of the body. Principles of self-organization do not account satisfactorily for the overall homuncular map. These results may serve to alert computational modelers that intrinsic developmental factors can override simple rules of plasticity.

1.  Introduction

Somatotopy in the primary somatosensory cortex (SI) provides the paradigm case of spatial adjacency, or topographic, mapping between the arrays of cells in cortical tissue and cutaneous mechanoreceptors. Penfield and coworkers compiled the familiar somatosensory homunculus (see Figure 1 and Table 1) in the mid-1950s by eliciting patients’ responses to electrical stimulation of their exposed cortex prior to surgical intervention for epilepsy.

Table 1:
Previous Work on the Foot-Genital Discontinuity in SI.
AuthorDetection MethodStimulation Method
Authors who located the penis discontinuously inferior to the foot in the paracentral lobule 
   Foerster (1936Subjective report from patient Electrical stimulation of cortex 
   Penfield and Boldrey (1937Subjective report from patient Electrical stimulation of cortex 
   Penfield and Rasmussen (1950Subjective report from patient Electrical stimulation of cortex 
   Penfield and Rasmussen (1968Subjective report from patient Electrical stimulation of cortex 
   Narici et al. (1991Magnetoencephalography Electrical stimulation of DNP 
   Guérit and Opsomer (1991Elcctroencephalography Electrical stimulation of DNPxs 
   Allison et al. (1996Electrodes in cortex Electrical stimulation of DNP and Electrical stimulation of cortex 
   Nakagawa et al. (1998Magnetoencephalography Electrical stimulation of DNP 
   Mäkelä et al. (2003Magnetoencephalography Electrical stimulation of DNP 
Authors who found the penis to be represented continuously with rest of the lower body in the postcentral gyrus 
   Pfeifer (1920Subjective report from patient and location of brain trauma site Tactile stimulation 
   Penfield and Jasper (1954Subjective report from patient Electrical stimulation of cortex 
   Bradley et al. (1998Electrodes in cortex and subjective report from patient Electrical stimulation of DNP 
   Redouté et al. (2000Positron emission tomography Erotic visual images 
   Kell et al. (2005fMRI Tactile stimulation 
   Moulier et al. (2006fMRI Erotic visual images 
   Mouras et al. (2008fMRI Erotic visual images 
AuthorDetection MethodStimulation Method
Authors who located the penis discontinuously inferior to the foot in the paracentral lobule 
   Foerster (1936Subjective report from patient Electrical stimulation of cortex 
   Penfield and Boldrey (1937Subjective report from patient Electrical stimulation of cortex 
   Penfield and Rasmussen (1950Subjective report from patient Electrical stimulation of cortex 
   Penfield and Rasmussen (1968Subjective report from patient Electrical stimulation of cortex 
   Narici et al. (1991Magnetoencephalography Electrical stimulation of DNP 
   Guérit and Opsomer (1991Elcctroencephalography Electrical stimulation of DNPxs 
   Allison et al. (1996Electrodes in cortex Electrical stimulation of DNP and Electrical stimulation of cortex 
   Nakagawa et al. (1998Magnetoencephalography Electrical stimulation of DNP 
   Mäkelä et al. (2003Magnetoencephalography Electrical stimulation of DNP 
Authors who found the penis to be represented continuously with rest of the lower body in the postcentral gyrus 
   Pfeifer (1920Subjective report from patient and location of brain trauma site Tactile stimulation 
   Penfield and Jasper (1954Subjective report from patient Electrical stimulation of cortex 
   Bradley et al. (1998Electrodes in cortex and subjective report from patient Electrical stimulation of DNP 
   Redouté et al. (2000Positron emission tomography Erotic visual images 
   Kell et al. (2005fMRI Tactile stimulation 
   Moulier et al. (2006fMRI Erotic visual images 
   Mouras et al. (2008fMRI Erotic visual images 

Note: DNP indicates Dorsal Nerve of the Penis.

Such topographic mapping is recognized as a common feature of the correspondence between the spatial organizations of receptors in many sensory epithelia and their targets in the central nervous system (Pickles, 1982; Udin & Fawcett, 1988; Kaas, 1991, 1997; Buonomano & Merzenich, 1998; Wong, 1999; Jones, 2000). The presence of topographic mapping in the nervous system has been interpreted on grounds that such an arrangement optimizes geometric, biophysical, and energy constraints (Laughlin & Sejnowski, 2003).

However, the genesis of topographic mapping is a subject of continuing debate between those who hold with the protomap or the protocortex position. The protomap view proposes that the spatially specific molecular signaling of neural progenitor cells in the proliferative zone establishes both spatial location and function of neurons within the primary subdivisions of cortex. By contrast, the protocortex view asserts that activity-dependent mechanisms alone give rise to topographic mapping in an otherwise homogeneous cortex (Killackey, Rhoades, & Bennett-Clarke, 1995; Wong, 1999; Sur & Rubenstein, 2005; Stiles, 2008). However, it is likely that both genetic and epigenetic factors contribute. The primary somatosensory region includes the separate architectonic fields 1, 2, 3a, and 3b. For reasons of probable homology with SI in other mammals, area 3b representation is referred to as SI in this view.
Figure 1:

The Penfield homunculus. The penile representation is located inferior to that of the foot. The face representation is inverted and displaced as a whole from that of the neck and posterior scalp. (Modified from Penfield & Rasmussen, 1950.)

Figure 1:

The Penfield homunculus. The penile representation is located inferior to that of the foot. The face representation is inverted and displaced as a whole from that of the neck and posterior scalp. (Modified from Penfield & Rasmussen, 1950.)

1.1.  Homuncular Discontinuities.

The familiar somatosensory homunculus (Penfield & Rasmussen, 1950) contains two notable discontinuities in SI: between the hands and the face and between the feet and the genitalia (see Figure 1). Farah (1998) assumed the protocortex position by proposing that the discontinuities occur because “mechanisms of self-organization, in combination with the normal position of the fetus in the womb will incline the map towards just this organization.” In the womb, the fetus generally has its hands abutting its face, and its feet the genitalia, creating coactivations of the respective body parts.

Farah's suggestion is supported by the generally accepted notions of cortical plasticity and self-organization (Hebb, 1949; Willshaw & von der Malsburg, 1976; Kandel & O'Dell, 1992; Florence et al., 1996; for a review of theoretical approaches to map development, see Goodhill, 2007) and by experiments entailing the simultaneous activation of body parts, which have revealed integrated, overlapping receptive fields in monkeys (Clark, Allard, Jenkins, & Merzenich, 1988; Wang, Merzenich, Sameshima, & Jenkins, 1995). Furthermore, computer simulations of the fetal position, using a Hebbian variant of Kohonen's self-organizing neural net, have provided an “existence proof” for the plausibility of Farah's proposal (Stafford & Wilson, 2006).

A review of recent literature reveals, however, that there is in fact no discontinuity in the genital representation in SI for cutaneous sensations (summarized in section 2). An analysis is presented of body parts that might be costimulated in utero and be expected to lead to somatotopy (see section 3). It is concluded that the rule that generally applies for the refinement of topographic mapping (Kandel & O'Dell, 1992) is inapplicable across the hand-face boundary in SI.

The displacement of the face representation from that of the neck and posterior scalp (see Figure 1) is explored in section 4, and it is suggested that this results from separate innervation (or parcellation) and development of the sensory fibers innervating the face from those innervating the rest of the body. With cutaneous somatotopy present elsewhere in the body, I propose that the boundary containing the facial representation constitutes the only homuncular discontinuity in SI.

Such a finding serves also to alert computational modelers of neuronal dynamics to pay heed to possible underlying developmental constraints, since computational models are inevitably limited by their axiomatic bases. Innervations within the oral cavity are not addressed.

2.  The Foot-Genital Discontinuity

Previous work on the localization in SI of sensations from the male genitalia is summarized in Table 1. The Penfield homunculus (Penfield & Rasmussen, 1950) sites the penile representation in SI discontinuously inferior to that of the foot, in the paracentral lobule of the mesial wall (see Figure 1).

However, an analysis of previous investigations that used a diversity of techniques for localizing brain activation in conjunction with (1) tactile stimulation of the penile skin (Pfeifer, 1920; Kell, von Kriegstein, Rösler, Kleinschmidt, & Laufs, 2005), (2) electrical activation of the dorsal nerve of the penis (DNP) (Guérit & Opsomer, 1991; Narici et al., 1991; Allison, McCarthy, Luby, Puce, & Spencer, 1996; Bradley, Farrell, & Ojemann, 1998; Nakagawa et al., 1998; Mäkelä et al., 2003), (3) the presentation of erotic images (Redouté et al., 2000; Moulier et al., 2006; Mouras et al., 2008), and (4) electrical stimulation of the cortex (Foerster, 1936; Penfield & Boldrey, 1937; Penfield & Rasmussen, 1950,1968; Penfield & Jasper, 1954; Allison et al., 1996) reveals at least two separate loci in SI dedicated to sensations arising from the penis. Those for cutaneous touch, which the somatosensory homunculus is intended to represent, are indeed located somatopically with the thighs and lower trunk.

It would appear that Penfield and coworkers and many of those using electrical activation of the DNP localized sensations of tumescence, which arise from the engorgement with blood of erectile tissue, discontinuously in the paracentral lobules (Penfield & Jasper (1954), revised the earlier findings of Penfield & Rasmussen (1950), and sited the penile representation continuously with that of the lower trunk and thigh in the post-central gyrus). The penile representation proposed by Bradley and coworkers (1998), although stated to be continuous with the trunk and thigh, was exaggerated, and extended into the mesial wall. This issue has been discussed by Kell and coworkers (2005). Electrical stimulation of the population of axons carried in the DNP can simultaneously activate myelinated cutaneous and slow, narrow Aδ fibers that carry sensations of tumescence (Nakamura et al., 1998; Georgiadis & Kortekaas, 2009) and lead to ambiguous results.

In sum, although many standard texts depict a foot-penile discontinuity (Styles, 2005; Purves et al., 2008), cutaneous sensations from the penis are represented continuously with those of the adjacent body parts in SI.

To summarize, there appears to be no disjunction in the penile representation in SI for cutaneous sensation. Previously reported penile representation in the paracentral lobule may be attributed not to cutaneous sensations but to those of tumescence. Georgiadis and Kortekaas (2009) support this view.1

3.  Analysis and Further Considerations

Despite there being frequent foot-penile contact in utero, penile somatotopy with the lower trunk and thighs is observed in SI. Furthermore, although there is costimulation of the face and the neck where they abut in the body, somatotopy is absent in SI between the face representation and that of the neck. Similarly, costimulation at the face and posterior scalp boundary does not lead to somatotropy in their representations in SI (see Figure 1). The overall findings are:

  • • 

    Foot-penile costimulation in utero, no SI adjacency

  • • 

    Neck-face/face–posterior scalp costimulation in utero, no SI somatotopy

  • • 

    Hand-face costimulation in utero, SI adjacency present

From these findings, we can surmise that costimulation and somatotopy in SI representation cannot be causally linked. Thus, even at this level of analysis, we may infer that the above data are at variance with Farah's proposal for the origin of homuncular discontinuities. These results are further considered below.

3.1.  Simultaneous Firing and Somatotopy.

Kandel and O'Dell (1992) have proposed molecular mechanisms to support the finding that simultaneous activity in adjacent presynaptic retinal ganglion axons leads to a refinement of retinotopy in subcortical nuclei. Such trophic mechanisms have been widely invoked to account for the pruning of inappropriately targeted axons (Purves, 1994; Wong, 1999). Applied to the somatosensory system, the coactivation of adjacent mechanoreceptors would refine cortical somatotopy and might be thought to support Farah's suggestion that frequent hand-face contact will place the face representation adjacent to that of the hand.

However, a hand-face contact event in utero would coactivate two distinct groups of mechanoreceptors—one group in the hand and the other in the face. On subsequent hand-face contacts, the same two groups of mechanoreceptor cells might not fire simultaneously because the hand is free to move over the face. Such hand-face contact events might create somatotopy separately in the hand and in the face, but not across the hand-face boundary in SI. The situation is the same in the case of foot-genital contact, where the feet are free to move over the genital region. However, as shown in section 2, there is no somatotopy present in SI between the foot and the penis representations. As such, hand-face adjacency in SI is likely to be generated by other causes.

This view is reinforced by findings in congenital amelics (e.g., thalidomide teratogens) studied by Flor et al. (1998) and Montoya et al. (1998), who examined the homuncular organization in individuals with only one affected upper limb. The frequency of prenatal hand-face contact in these cases may be expected to be asymmetrical. Localization of cortical activation generated by cutaneous touch, using brain-imaging techniques, nevertheless allowed bilateral hand-face adjacency to be inferred in SI despite unilaterally affected upper limbs.

In the case of the experiments entailing costimulation by Clark et al. (1988) and Wang et al. (1995), the body parts whose representations were found to be merged had not been free to move independently. In the former experiment, the digits were constrained and costimulated, and in the latter, the digits had been surgically fused.

In the examples (Clark et al., 1988; Wang et al., 1995), the body schema (Maravita, Spence, & Driver, 2003; Price, 2006) associated with proprioception and cutaneous sensation (whose nervous pathways are co-parcelled) would adapt to reflect body-part fusion in SI. However, in the case of hand-face contact, the body schema would be at variance with a bodily configuration representing hand-face fusion. Furthermore, costimulation of the facial skin and that of the posterior scalp and the neck does not lead to somatotopy across their respective boundaries with the face, even though the body schema would support such a configuration.

This finding casts doubt on the universal applicability of Kandel and O'Dell's (1992) mechanism for the refinement of topographic maps and reinforces the view that hand-face adjacency in SI arises from other causes. These are explored below.

4.  Face Parcellation

The overall map of the human somatosensory homunculus for cutaneous sensations that emerges from the results obtained thus far can be interpreted as follows. There exist two distinct regions exhibiting cutaneous somatotopy in SI: the face representation and that of the rest of the body. I observe that the face representation is inverted and displaced as a whole from that of the neck and posterior scalp to lie discontinuously adjacent to that of the thumb (this anomaly is also noted by Penfield & Rasmussen, 1968, and Itomi, Ryusuke Kakigi, Hoshiyama, & Watanabe, 2001; see Figure 1 here). The soundness of this classical finding by Penfield and coworkers has been confirmed more recently by Moulton et al. (2009), who charted the two-dimensional onion skin face representation in SI using fMRI (see section 4.1).

In the owl monkey, the face representation is displaced from that of the neck but is not inverted with respect to that of the body. Here, the representation of the chin vibrissae is adjacent to that of the glabrous thumb in area 3b (Merzenich, Kaas, Sur, & Lin, 1978). Cortical face representation in many rodent species, by contrast, is continuous with that of the neck. It should also be noted that in the human homunculus, the part of the face the thumb abuts is the vertex of the head (I am grateful to P. D. McLeod for this observation), not the mouth, with which it has frequent contact during the fetal stage (Myowa-Yamakoshi & Takeshita, 2006).

Factors underlying separate facial representation are sought through an analysis of facial skin innervation and the time of onset of its sensory function in relation to those of the rest of the body.

4.1.  Anatomy.

Cutaneous sensations from peripheral mechanoreceptors in the face are carried to the thalamus in the trigeminal somatic sensory system. Those originating in the rest of the body project separately in the dorsal column-medial lemniscus pathway (Purves et al., 1997; Larsen, 2002; Upadhyay, Knudsen, Anderson, Becerra, & Borsook, 2008; see Figure 2).
Figure 2:

A schematic representation of the trigeminal and dorsal column-medial lemniscus pathways. Afferents from cutaneous mechanoreceptors in the face and the rest of the body form separate cortical representations. The somatosensory homunculus is depicted at the top-left of the diagram. For further details, see section 4.1. (Adapted from Purves et al., 1997, Figure 8.6, and Kell et al., 2005, Figure 3.)

Figure 2:

A schematic representation of the trigeminal and dorsal column-medial lemniscus pathways. Afferents from cutaneous mechanoreceptors in the face and the rest of the body form separate cortical representations. The somatosensory homunculus is depicted at the top-left of the diagram. For further details, see section 4.1. (Adapted from Purves et al., 1997, Figure 8.6, and Kell et al., 2005, Figure 3.)

Afferents from cutaneous receptors in the three well-defined facial zones of the onion skin representation (Kunc, 1970; Borsook, DaSilva, Ploghaus, & Becerra, 2003; Moulton et al., 2009) are carried in the three components of the trigeminal somatic sensory system (ophthalmic: V1, maxillary: V2 and mandibular: V3), providing somatotopic organization related to the afferent projections of the three components (Borsook et al., 2003). These zones cover the bulk of the face and mouth (Moulton et al., 2009). All sensory fibers from these pathways make first-order synapses in the trigeminal nucleus (main V), which has detailed maps of these components. There is also evidence that an inverted facial representation is present in main V (Brodal, 1981). The sensory outputs from main V that originate in the facial zones are carried by the trigeminal lemniscus, and make second-order synapses in the ventral posterior medial (VPM) nucleus of the thalamus.

The afferents from cutaneous receptors from the rest of the body, including the posterior scalp (innervated by cervical spinal nerves, C2 and C3) and part of the external ear (Nihashi et al., 2002, 2003), are carried to the thalamus by the dorsal column-medial lemniscus pathway. First-order synapses form in the two dorsal column nuclei in the medulla (the cuneate and gracile nuclei, innervating, respectively, the upper and lower parts of the body), and the medial lemniscus carries axons from these nuclei to form second-order synapses in the ventral posterior lateral nucleus of the thalamus (VPL). This nucleus has ordered maps of the remainder of the body (Purves et al., 1997).

From VPM and VPL in the thalamus, separate thalamocortical pathways target different regions of somatosensory cortex. These pathways have been explored in monkeys and provide further support for separate face parcellation:

  • • 

    Jain, Catania, and Kaas (1998) report that a morphologically distinct septum separates the hand-face boundary in cortex.

  • • 

    Lesion studies (Jones, Manger, & Woods, 1997) showed that silenced cortical hand representations were not encroached on by adjacent face representations.

  • • 

    Hand-face adjacency is reported to exist in the ventroposterior nucleus (VP) of the thalamus (Jain, Qi, Collins, & Kaas, 2008). However, lemniscal afferents (to VPL) and principal trigeminal afferents (to VPM) do not overlap across these two subnuclei of VP (Raussel, Bickford, Manger, Woods, & Jones, 1998).

  • • 

    Similarly, in the same study (Raussel et al., 1998), injections of anterogradely transported tracers in VPM and VPL showed that cortical projections from these thalamic nuclei targeted distinct nonoverlapping regions in SI (representing separately the face and the rest of the body).

  • • 

    Horizontal corticocortical connections, which are extensive within dorsal column-lemniscal and trigeminal representations, do not cross the border between the hand and face representations (Manger, Woods, Muñoz, & Jones, 1997; Fang, Jain, & Kaas, 2002). Similar results are found in the thalamus (Fang et al., 2002).

  • • 

    VPL and VPM are separated by a prominent cell-sparse border of white matter, the arcuate lamella, dividing face representation from that of the rest of the body (Jones, 2000).

These findings reinforce the proposal of a separate parcellation of the trigeminal pathway from those innervating the rest of the body.

In chronically deafferented animals, however, an invasion of the jaw representation into that of the body's has been previously reported (12 or more years after surgery) (Brown, 1974; Jain et al., 2008) and attributed to expansions of regions innervated by the mandibular nerve, which overlaps input from the upper cervical nerve representation in macaques (Manger et al., 1997). This phenomenon is discussed by Jones (2000) in relation to atrophy of the arcuate lamella.

The septum referred to in Jain et al. (1998) differs from those found at partial discontinuities in receptor sheets that follow the rule: “The terminations of sensory projections with discorrelated activity segregate” (Catania & Kaas, 1995). Rather, it appears to be of another kind that delimits mechanically the spread of new connections in adult brains (Catania & Kaas, 1995). Both Jones (2000) and Jain et al. (2008) remark that normal cortical tissue is capable of setting up boundary conditions that effectively localize representation of body parts, notably the face.

In sum, what appears as the separate face representation in the homunculus is innervated by the separately parcelled trigeminal pathway. The posterior scalp and the neck are innervated by C2 and C3 (Larsen, 2002), not by the trigeminal nerve. These body parts mark the limits beyond which the face is displaced as an island.

4.2.  Ontogeny.

Topographic mappings emerge sequentially, beginning from the array of cutaneous mechanoreceptors at the periphery and ending in cortex, with somatotopy generally maintained throughout the neuroaxis (Killackey et al., 1995; Scott & Atkinson 1999; Rubel, 2004).

Separate face parcellation is reflected also in its earlier onset of function compared to the rest of the body. During human gestation, at 7.5 weeks gestation age (g.a.), the mouth is the first location that elicits motor responses to cutaneous stimulation; by contrast, the first bodily response occurs at 10.5 weeks g.a. (Brown, 1974). The earlier development and consolidation of the trigeminal pathway is consistent with its separated parcellation in cortex.

5.  Conclusion

The analysis leads to the proposal that the somatosensory homunculus results from two distinct, separately developing nervous pathways: one innervating the face and the other the rest of the body.

These separately parceled bundles of nerves, originating in the cutaneous mechanoreceptors, synapse in different sets of intervening nuclei and form separate representations in cortex. The boundary between these two regions constitutes and creates the homuncular discontinuities.

Face-posterior scalp/neck disjunction in SI is consistent with this view. The irrelevance of the frequency of hand-face contact in utero in determining the overall homuncular plan can be supported on two counts. Such contacts can create somatotopy separately only in the hand and in the face (as explained in section 3.1). Furthermore, even if body schema constraints were removed, there remain boundaries between these distinct bundles of nerves across which rules of plasticity do not apply.

Computational modelers may do well to take note that these findings point to the existence of intrinsic developmental factors, other than simple epigenetic rules, that determine the overall form of the homuncular map.

Acknowledgments

For their comments on the manuscript, I thank X. Barandiaran, M. A. Boden, R. J. Keynes, S. Koelsch, P. D. McLeod, T. Nowotny, J. K. O'Regan, J.V. Stone, and A. S. Woodward.

Note

1

The original Penfield homunculus, reproduced in Figure 1, wrongly represents face and body parts in the ipsilateral hemisphere. This error is repeated in other work cited here (Bradley et al., 1998, Figure 6; Kell et al., 2005, Figure 3; and Nakamura et al., 1998, Figure 3).

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