Sensory representation in the neocortex of the mole, Scalopus aquaticus

EXPERIMENTAL

Sensory

NEUROLOGY

27, 554-563 (1970)

Representation

in the

Scalopus TRUETT

ALLISON

Neocortex

of

the

Mole,

aquaticus

AND HENRY

VAN TWYVER 1

Veterans Administration Hospital, West Haven, Connecticut06516, and Yale University School of Medicine, New Haven, Connecticut Received February

24, 1970

The neocortex of the mole, Scalopus aquaticus, was expored by the evoked potential technique to determine visual, somatic, and auditory areas. No visual evoked response could be recorded in any animal. In agreement with anatomical studies, we conclude that there is essentially no visual cortex in the mole. The primary somatic area appears to have shifted posterolaterally, compared to another insectivore, the hedgehog, possibly due to the absence of visual cortex. The auditory area in the mole is similar in location to that in hedgehog and rat. Introduction

Most zoologists and naturalists have considered the moles to be blind or nearly blind (6, 7, 11, 14). However, recent stuudies indicate that the European mole (TaZ$a euro/~~ea) has an essentially normal retina (11) and can make a light-dark discrimination (10). To assesspossible visual function in the eastern North American mole, ScaIopu.s aquaticus, we have attempted to record cortical visual evoked responses.Somatic and auditory responseswere recorded to delimit presumed visual cortex and to verify that recording conditions were favorable ; theseresults are also reported. Methods

Nine moles weighing 58-95 g were anesthetized with sodium pentobarbital 30 mg/kg ip or alpha chloralose 50 mg/kg ip with small supplemental dosesas required. The skull overlying neocortex was exposed. In a preliminary experiment an attempt to remove the bone fat- recording directly from the brain proved fatal. We obtained excellent recordings by carefully thrusting Grass subdermal needle electrodes through the thin skull until the tip was judged to touch the dura mater. In this way, damage to the brain was minimized and problems of drying and cooling of the brain were 1 Supported by USPHS Grant MH-05286 and by the Veterans Administration. thank W. R. Gaff and T. Fisher for advice and assistance. Dr. Van Twyver Veterans Administration Research Associate in Psychology. 554

We is a

MOLE

CORTEX

555

avoided. Evoked responses were recorded from four locations simultaneously. They were averaged by an analog device (13)) displayed on a fourchannel oscilloscope, and photographed. When the maximum amplitude focus was located for a given stimulus, that electrode was left in place so that responses obtained later, at possibly different levels of anesthesia, could be compared quantitatively. At least three averaged responses were obtained at each location. Somatic, auditory, and visual averaged responses were composed respectively of 5, 20, and 30 individual responses. Body temperature was maintained at 34 -+ lC, approximating the normal temperature in this species (2). Somatic stimuli were 0.1-0.5 msec square-wave pulses delivered via needle electrodes placed subdermally in hind limb, forelimb, or snout. Stimulus intensity was just above twitch threshold for limb stimulation. Click stimuli were delivered via a loudspeaker located approximately 20 cm from the animal’s head. Click intensity, measured with a type 1556-B General Radio impulse noise analyzer and type 412 Scott noise level meter, was 105-110 db re 0.0002 microbar. Intense light flashes from a General Radio strobe lamp were directed through a window in the recording chamber primarily to the eye contralateral to the recording electrodes ; the eye-to-lamp distance was approximately 30 cm. The fur normally covering the eye was carefully shaved before recording. The skin covering the eye was left intact. At the end of each experiment the brain was perfused and the skull removed for verification of electrode placements. In most instances the true location was quite close to the intended location because neocortical boundaries could be seen through the thin skull. In size and general appearance the brain of Scalopz~ is very similar to that of the hedgehog (Fig. 1 in Ref. 9). For each animal, 90 and 50% (of maximum response amplitude) isopotential contours were plotted on an outline of the neocortex. The outline was drawn directly from dorsolateral views of brains enlarged with a projector. In some experiments the responsive area boundaries were not determined completely; in these cases the estimated boundary is indicated by hatching not enclosed by a line. Results

Figure 1 shows typical responses evoked by auditory and somatic stimuli. The response consisted of the classical short-latency positive-negative waves of primary projection cortex. The negative wave was often small or absent under sodium pentobarbital. and under chloralose it was usually obscured by a second positive wave; thus, only the short-latency positive wave was measured to determine responsive areas.

556

ALLISON

,lND

VApi

TR’YVEK

forelimb

I

snout

I

1. Characteristic auditory (left) and somatic (middle and right) evoked responses from the neocortex of the mole. For the primary positive wave, average peak latencies and range of latencies (in msec) for all animals were : auditory, 20 (12-23) ; somatic snout, 12 (11-13) ; forelimb, 18 (15-24) ; hind limb, 25 (22-27). In this and following figures positive is recorded upward, recording is referential to the skull anterior to the brain. Time: 50 msec. Voltage, auditory, 50 pv; somatic, 400 pv. FIG.

The responsive areas to somatic stimuli are shown in Figs. 2-4. The hind limb is represented medially, the forelimb more lateral, and the snout ventraIly in a region just above the rhinal sulcus. Despite the IikeIihood of some volume conduction through the intact dura and bone, the responsive areas were often remarkably focalized (e.g., Fig. 2A), even with the very large responsesrecorded under chloralose. Figures 3 (above) and 4 (above) are examples of somewhat wider distributions to forelimb and snout stimulation.

The

smaller

bind

limb areas sometimes

seen may be more

apparent

than real since we did not explore the medial surface. These responsive areas correspond

to Woolsey’s

( 16) somatic area I (SI)

.

In several animals longer latency responseswere recorded to forelimb and hind-limb stimulation in a region within or near the snout area. Presumably this region corresponds to SII ; however, these responses were not studied systematically. Only a single evoked response focus was seen to snout stimulation. Under chloralose anesthesia 30- to 50-msec peak area” responses (1, latency positive waves, possibly similar to “association 15), were seen in and around primary projection cortex. However, no association areas could be delimited as the responsive regions were variable between animals and in the sameanimal to different stimuli. Click-evoked responses were considerably smaller in amplitude than somatic responses (Fig. l), and in a few experiments no auditory responsescould be found. The region responding to click was very small in all animals (Fig. 5). The responsive area appeared to be within the somatic snout area with the exception of one animal (H) in which the auditory area was clearly posterior to the snout area. No responseswere seenoutside this primary focus.

JIOLE

557

CORTEX

FIG. 2. Somatic hind limb representation. Above. Example of highly focalized response. Below. Isopotential contour maps of all experiments. In this and following figures the area within which response amplitude was 90% or more of maximum amplitude is indicated by hatching; striped area indicates 50% region. Where boundaries could not be assessed quantitatively due to lack of recording points, the estimated

boundary

is indicated

by

lack

of

a border.

For

comparison

of

results,

animals

are

identified in the lower left corner of each figure. Attempts to record visual evoked responses in nine experiments (five under sodium pentobarbital, four under chloralose) were unsuccessful, even though many more summations were taken than for somatic and In all experiments the light was directed to the eye auditory responses. contralateral to the recording site, since in most specimens of Talfx optic nerve fibers decussate completely in the chiasm (10). Figure 6 shows results from one such experiment in which presumed visual cortex was explored under chloralose. In this example, a IOO-msec sweep was used to search for early response components. In all experiments a 500-msec sweep was also used to record possible long latency responses; none were

558

FIG.

large

ALLISON

AND

VAl\i

TWYVER

3. Somatic forelimb representation. Above, This evoked potential field. Below. Isopotential contour

is an example of a relatively maps of all experiments.

seen. Recordings were obtained from up to 18 locations in other experiments. ohservations were made on an unIn addition to these experiments, anesthetized animal with electrodes chronically implanted in parietal and occipital areas. Flashes at rates from @W/set did not induce photic driving. Nor could visual evoked responses be recorded from any electrode although auditory and somatic responses were readily recorded from the parietal leads. Discussion

The topographic organization of SI in the mole in that the hind limb is represented medially, the and the face laterally on the neocortical surface comparing these results with those obtained in the other insectivore studied to date, some difference is

is typically forelimb (Fig. 7). hedgehog apparent.

mammalian intermediate, However, in (9), the only In the hedge-

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CORTEX

559

FIG. 4. Somatic snout representation. Above. Responsive area in one animal. Below. Isopotential contour maps of all experiments.

hog the hind-limb representation is entirely on the medial surface, the forelimb is represented near the midline, and the nose area lies well above the rhinal sulcus. These areas occupy roughly the middle half of neocortex and are bounded anteriorly by the orbital sulcus. By contrast, in the mole the hind limb is represented at least in part on the lateral surface and the snout area is located just above the rhinal sulcus. These areas are, on the average, directly above the laterally directed “knee” of parietal cortex. In no experiment were responses recorded in the region of the orbital sulcus (in ScaZopus there is no clear orbital sulcus, but in some animals a shallow indentation can be seen where the sulcus would be expected). Thus in the mole area SI appears to be shifted laterally and posteriorly compared with its location in hedgehog, and posteriorly compared with the rat (16). It is possible, but we think unlikely, that this difference is attributable to diffzrences in methods of stimulation (shock stimuli versus Lende and Sadler’s discrete tactile stimuli) or recording. Rose (12) studied the cortical

560

FIG.

contour

ALLISON

5. Auditory area. Above. maps of all experiments.

AND

Responsive

VAN

area

TCVYVEK

in one animal.

Below.

Isopotential

cytoarchitecture of Talpa. Yo striate cortex (area 17) was seen, its place being taken by cortex resembling the retrosplenial region (area 30). In other mammals. including hedgehog, this region lies on the medial surface (5) and corresponds roughly to the region from which Lende and Sadler (9) recorded hind-limb responses. Furthermore, in Talpa (12) the postcentral-parietal region (areas 5 and 7) is located posteriorly and extends more laterally compared to its position in hedgehog (5). Thus, the cytoarchitectonic and evoked response data agree in showing a posterolatera1 displacement of somatic cortex in the mole. Perhaps this posterolatera1 shift of SI results from the apparent degeneration of visual cortex in this species ( 12 : and see below ) . The location of the auditory area in the mole (Figs. 5 and 7 j , hedgehog (9) and rat (16 ) is very similar. In hedgehog there is considerable overlap of auditory and somatic nose areas. In the mole this overlap appears to

MOLE

CORTEX

561

I 2 3 4 5 6

H <

7 8

Fig. 6. Visual stimulation. No visual responses were present at these locations others recorded in the same experiment. Chloralose anesthesia, 50 mgjkg. Note recording sensitivity compared with somatic and auditory recordings.

FIG.

smoothed

and high

7. Summary of somatic and auditory areas. In each case the border is a curve encompassing the 50% isopotential areas of all individual experiments.

be virtually complete, apparently due to the posteroalteral shift of SI. In only one experiment was the auditory area clearly posterior to the somatic snout area. We were unable to record visual evoked responses in any animal, whether unanesthetized or anesthetized with sodium pentobarbital or chloralose. These negative results are, naturally, not conclusive. It is possible

562

ALLISON

AND

VAN

TWYVER

that different anesthetic levels or other experimental changes would have allowed the recording of visual responses. However, our failure to record visual evoked responses under chloralose is particularly significant since this anesthetic considerably potentiates early components of sensory-evoked responses. We conclude that in the mole no visual cortex is present as determined by the evoked-potential method. This conclusion is compatible with anatomical results, although there has been little study of the visual system of Scalopus. Somewhat more is known of the visual system of a similar species, Talpa europaea, and in the following discussion it will be assumed that these results are essentially correct also for Scalopus. In Talpa there are about 200 fibers in each optic nerve (10, 11). Lund and Lund (lo), using the Nauta method after unilateral eye enucleation, found terminal degeneration in the dorsal lateral geniculate nucleus (LGN) in only two of six animals. Some evidence of degeneration was found in ventral LGN in all animals ; this region, however, does not project to cortex (3). Based on study of normal material, Johnson (8) found in .‘?c~opus that only a few optic tract fibers terminate in dorsal LGN, described as a very small area consisting only of small, scattered cells (4). Even if the dorsal LGN projects to cortex (this has not been established, and as noted above, there is no striate cortex in Talpa) the anatomical results show that visual input to cortex is feeble at best and probably nonexistent in some animals. Our failure to record visual evoked responses from neocortex is therefore not surprising. In Talpa the pretectum is the primary optic center (10). This species could be trained to make a light-dark discrimination (10). Whatever visual capacity Scalopus may have is also likely mediated by the pretectal area, or possibly by the inferior colliculus (8). Slonaker ( 14) found that the eye of Scalopus is considerably more degenerate than that of Talpa. He also carried out several crude behavioral tests, and concluded that “the eye of the common mole is quite incapable of being stimulated to such a degree as to cause any modification in the activity of the animal.” Adequate behavioral tests of the kind employed with Ta.Zpa (10) will be required to verify Slonaker’s conclusion. References D., and A. FESSARD. 1963. Thalamic integrations and their conat the telencephalic level. Progr. Brain Rcs. 1: 115-148. 2. ALLISON, T., and H. VAN TWYVER. 1970. Sleep in the moles, Scalopns aquaticus and Cottd$ura cristata. Exp. Neural. 27 : 564579. 3. ARIENS KAPPERS, C. U., G. C. Huber, and E. C. CROSBY. 1936. “The Comparative Anatomy of the Nervous System of Vertebrates, Including Man.” Vol. 2 : Macmillan, New York. 4. BAUCHOT, R. 1959. Etude des structures cytorachitectoniques du dienciphale de 1.

ALBE-FESSARD,

sequences

MOLE

5. 6.

7. 8. 9. 10. 11. 12. 13. 14. 15. 16.

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Talfia europaea (Insectivora talpidae). Acta .&at. 38 : 90-140. K. 1909. “Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues.” Barth, Leipzig. GAUGHRAN, G. R. L. 1954. A comparative study of the osteology and myology of the cranial and cervical regions of the shrew, Blarina breticauda, and the mole, Scalopus aquaticus. Misc. Pub. Mus. Zool. Univ. Mich. 80: l-82. GODFREY, G. K., and W. P. CROWCROFT. l%O. “The Life of the Mole.” Museum Press, London. JOHNSON, T. N. 1954. The superior and inferior colliculi of the mole ([email protected] aquaticus machrinus). J. Camp. Nezlrol. 101: 765-799. LENDE, R. A., and K. M. SADLER. 1967. Sensory and motor areas in neocortex of hedgehog (Eriaaceus). Brain RES. 5: 390-405. LUND, R, D., and J. S. LUND. 1965. The visual system of the mote, Talpa europaea. Exp. Neltrol. 13: 302-316. QUILLIAM, T. A. 1964. Special features of the eye of the mole (Talpa ezlvopaea). Anat. Rec. 148: 396. ROSE, M. 1912. Histologische Lokalisation der Grosshirnrinde bei kleinen Saugetieren (rodentia, insectivora, chiroptera) . J. Psychol. Neural. 19 : 391-479. ROSNER, B. S., T. ALLISON, E. SWANSON, and W. R. GOFF. 1960. A new instrument for the summation of evoked responses from the nervous system. Electroencephalogr. Clin. Newopltysiol. 12 : 745-747. SLONAKER, J. R. 1902. The eye of the common mole, Scalops aquaticus machrinus. J. Camp. Neurol. 12 : 335-366. THOMPSON, R. F., R. H. JOHNSON, and J. J. HOOPES. 1963. Organization of auditory, somatic sensory, and visual projection to association fields of cerebral cortex in the cat. J. Nertropitysiol. 28 : 343-364. WOOLSEY, C. N. 1958. Organization of somatic sensory and motor areas of the cerebral cortex, pp. 63-81. In “Biological and Biochemical Bases of Behavior.” H. F. Har!eJw and C. N. Woolsey [eds.] Univ. Wisconsin Press, Madison, Wisconsin BRODMANN,