Download Somatosensory System Organization and Texture Sensation in Rats

440 Chapter 21
Somatosensory System Organization and Texture
Sensation in Rats and Mice
The Whiskers of Mice and Rats
How do impulses from skin receptors eventually lead to the sensation (i.e., the registration
of the elemental properties) and perception (i.e., recognition of the identity and meaning of the sensation) of the things that we contact? As a first example, we use the sensory
pathways originating in the whiskers of mice and rats to illustrate the main principles of
the organization and function of touch. We then show how these principles apply to sensation and perception in primates.
Mice and rats are active in dark environments and have poor vision; their survival depends
on the sense of touch. Through the whiskers, the brain builds up percepts of objects: their
position, size, shape, and texture.41 The heart of the tactile system is an array of some 35 long
whiskers on each side of the face, thick hairs that the animal flicks forward and backward
(there are also shorter, and less mobile hairs packed densely around the nose and lips that the
animal can use to collect additional information).42 Contact with an object activates mechanoreceptor terminations located in the whisker follicles, giving rise to neuronal signals (see
Figure 21.2B). The first study to utilize the whiskers as an object of research was carried out
by S. Vincent in 1912 for her Ph.D thesis at the University of Chicago (using rats captured in
the city!).43 She built an elevated labyrinth and found that the time required to run from the
start to the end of the maze and the number of errors (for example, stepping into dead-end
arms) increased dramatically when whiskers were clipped. The rats were slowed by the need
to feel the edge of the platforms with their feet rather than with their whiskers.
41
Diamond, M. E. et al. 2008. Nat. Rev.
Neurosci. 9: 601–612.
42
Brecht, M., Preilowski, B., and Merzenich,
M. M. 1997. Behav. Brain. Res. 84: 81–97.
43
Vincent, S. B. 1912. Behav. Monogr. 1-82.
44
Welker, E., and van der Loos, H. 1986.
J. Neurosci. 6: 3355–3373.
Magnification Factor
The behavioral importance of the rodents’ whiskers goes hand in hand with the richness
of the skin innervation. The whisker pad is the most densely supplied skin area of the body
studied so far—about 200 trigeminal ganglion neurons innervate each whisker follicle.44 In
Figure 21.6A, it is evident that the primary somatosensory cortex occupies a greater territory
(A)
(B)
Posterior
Anterior
Primary somatosensory cortex
Somatosensory, whiskers
Primary visual cortex
Primary auditory cortex
(C)
α
β
γ
A1
A2 A3
A4
B1
B2 B3 B4
C1
C2
D1
D2 D3
δ
E1
C3 C4 C5
E2
D4
E3
D5 D6
E4
E5
E7
E6
D6
D5
D4
D3
D1 D2
FIGURE 21.6 Cortical Representation of
the Whiskers in Rats and Mice. (A) Relative
positions and sizes of primary sensory cortical
fields. (B) Barrels in the mouse somatosensory
cortex visible in a tangential section through
layer IV. The dark rings are the cell-dense walls
of the barrels. (C) Arrangement of the barrels
in the left hemisphere of a rat, with each barrel labeled by its corresponding whisker. In the
sketch on the right, whiskers D1 to D6, which
project to barrels D1 to D6 are shown full-length.
The follicles of other whiskers are depicted as
dots. (B after Blakemore, 1977.)
©2011 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.
Touch, Pain, and Texture Sensation 441
than do the primary sensory fields for vision and audition. And within primary somatosensory cortex, the whisker field is disproportionately large. Although this can be interpreted
as a greater magnification of the whiskers’ cortical representation with respect to that of
other body parts (i.e., in terms of square millimeters of skin projecting to square millimeters of cortical surface), it can also be interpreted as conservation, across body areas, of the
relationship between receptor density and cortical territory. In other words, the number of
tactile receptors projecting to each square millimeter of cortical surface is held constant.
As a result, the richly innervated whisker follicles gain a large territory.
Topographic Map of the Whiskers and Columnar Organization
To visualize the organization of the mouse somatosensory cortex, Woolsey and van der
Loos45 separated the cerebral cortex from the underlying structures. Then, they flattened the
curved cortex between two slides and sectioned the slab in a tangential plane that yielded
a large horizontal expanse of layer IV in a single section. Once the tissue was stained, distinct clusters of densely packed neurons were visible. The grid-like arrangement of the 35
clusters resembled wine casks, calling out for the name barrels (Figure 21.6B). The insight
of Woolsey and van der Loos was that the spatial arrangement of the barrels replicates
exactly the spatial arrangement of the whiskers on the snout. The authors concluded that
the barrel field is a map of the whiskers on the contralateral snout. Every whisker on the
snout was given a label (e.g., D3) and could be readily matched with one cortical barrel
(again, D3). Within a few years, the prediction of a connection from each whisker to its
own cortical barrel was extended from mice to rats and confirmed by many physiological
studies.46–49 Thus, the receptive fields of the neurons in barrel D3 are centered on the socalled principal whisker, D3. Whiskers surrounding the principal whisker may also excite
cells to a lesser degree. Neurons in the layers above and below layer IV, which receive their
main sensory input from layer IV, also receive a strong input from the principal whisker.46
So, the neuronal population extending through all layers forms a cortical column associated with a single whisker, a functional unit anchored by the layer IV barrel.
Because two whiskers that are adjacent to each other on the animal’s face are represented in adjacent cortical barrels, the barrel field constitutes a topographic map (Figure
21.6C). Beyond the special case of whiskers, it is common to refer to a brain representation
as a “map” whenever the spatial relationship among sensory receptors is conserved in the
central representation of the sense organ. A historical note on the discovery of cortical
somatosensory maps is given in Box 21.1.
The map of cortical columns serves to organize the storage of sensory experiences. One
demonstration is provided by an experiment in which, to begin, all whiskers except one
were trimmed from the snout of the rats (Figure 21.7A). Then, the animals were trained,
in the dark, to perch on one platform, extend the intact whisker across a gap to touch
and, thus, localize a second platform, and jump across the gap to reach a reward. Next,
the trained whisker was clipped off and a previously clipped whisker was fixed with glue
to a different whisker stub (Figure 21.7B). When retested, the number of trials necessary
to reacquire the task was found to increase as a function of the distance between the site
of the trained whisker and the new (i.e., attached) whisker (Figure 21.7C). Moreover, the
transfer of learning between any two whisker locations was perfectly explained by the
spatial distribution of physiological activity within the barrel field map (Figure 21.7D).
This experiment suggests the presence of a sensory memory trace governed by the precise
topography of the sensory receptors.50
Map Development and Plasticity
When a strain of mice is bred to have different numbers of whiskers, the barrel field differs in precise correspondence with the face; thus, extra whiskers (or missing whiskers)
are accompanied by extra (or missing) barrels in the matching part of the barrel field.51,52
Destruction at birth of a whisker follicle will cancel that whisker’s module from all maps
in the ascending sensory pathway.53 But once the anatomical connection between one
whisker and its corresponding cortical barrel is established a few days after birth, that barrel remains fixed throughout life.
45
Woolsey, T. A., and van der Loos, H. 1970.
Brain. Res. 17: 205–242.
46
Armstrong-James, M., Fox, K., and DasGupta, A. 1992. J. Neurophysiol. 68:
1345–1358.
47
Simons, D. J. 1978. J. Neurophysiol. 41:
798–820.
48
Welker, C. 1976. J. Comp. Neurol. 166:
173–189.
49
Petersen, R. S., and Diamond, M. E. 2000.
J. Neurosci. 20: 6135–6143.
50
Harris, J. A., Petersen, R. S., and Diamond,
M. E. 1999. Proc. Natl. Acad. Sci. USA 96:
7587–7591.
51
van der Loos, H., and Dorfl, J. 1978.
Neurosci. Lett. 7: 23–30.
52
van der Loos, H., Dorfl, J., and Welker, E.
1984. J. Hered. 75: 326–336.
53
Jeanmonod, D., Rice, F. L., and van der
Loos, H. 1977. Neurosci. Lett. 6: 151–156.
©2011 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.
442 Chapter 21
(A)
(B)
Trained
whisker
Prosthetic
whisker
(D)
D2 response
C2 response
B2 response
10
5
0
Trained
whisker
4
2
Immediate relearning
0
Accelerated relearning
No transfer of learning
D2 × C2
overlap 20.9
FIGURE 21.7 Role of the Cortical Whisker Map in Sensory
Learning. (A) In the gap-crossing task, the rat learned to identify, in
the dark, the location of a reward platform by making contact using
a single whisker, referred to as the “trained whisker.” In this drawing,
first it leans into the gap (upper sketch) and then it extends forward
to reach the target (lower sketch). (B) The trained whisker (left) was
clipped off (middle) and a different whisker was fixed to a whisker
stump some specific distance from the stump of the trained whisker
(prosthetic whisker, right). (C) Schematic depiction of the whisker grid.
The speed at which the rat relearned the gap-crossing task depended
on the distance from the site of the trained whisker (T) to the site of
attachment of the new whisker, indicating that learning was localized.
(D) In the upper three plots, the number of action potentials (spikes
per trial) evoked by separate, brief movements of three different whis-
54
Andres, F. L., and van der Loos, H. 1985.
Anat. Embryol. (Berl.) 172: 11–20.
(Spikes per trial)2
6
Spikes per trial
(C)
D2 × B2
overlap 2.9
kers (D2, C2, and B2) is illustrated. The responses were measured
across a 10 × 10 grid of microelectrodes placed in the barrel cortex;
electrode positions are designated by gray dots. The lower two plots
indicate the degree of overlap in the cortical representation between
whisker pairs (D2 × C2, and D2 × B2). This is calculated by multiplying the separate responses to the two whiskers at each electrode;
thus the response scale is (spikes squared per trial) squared. Cortical
overlap is higher for the closer whisker pair (D2 × C2) than for the
more widely separated whisker pair (D2 × B2). The key result is that
the exact quantity of cortical overlap between the representations of
any two whiskers perfectly accounts for the degree of learning transfer between those two whisker sites. (After Harris et al.,1999.)
The topographic map at the level of cortex is not generated ad hoc from a disordered
input—rather, all along the pathway, the neighboring relations are received in an orderly
manner from the preceding level (the descending feedback projections mentioned earlier in
the chapter respect the same topographic order). Each barrel receives input from a discrete
barreloid in the ventroposterior medial nucleus of the thalamus; each thalamic barreloid
receives input from a barrelette in the brainstem trigeminal nucleus; and each barrelette
receives input from a whisker. During development the modular clustering appears in a
temporal sequence from periphery to cortex.54
Although the principal input to a given barrel is its topographically matched whisker,
neurons do respond to stimulation of neighboring whiskers, particularly in the column
of neurons above and below the layer IV barrel. These inputs form the surround receptive
©2011 Sinauer Associates, Inc. This material cannot be copied, reproduced, manufactured
or disseminated in any form without express written permission from the publisher.