A Neurologic Approach to Perceptual Problems

 Early Experience and Visual Information Processing in Perceptual and Reading Disorders. F.A. Young and D.B. Lindsley, eds., National Academy of Sciences, Washington, D.C., 151-156, 1970

Dr. Boynton has suggested that we might learn something more about perceptual problems by exploring the receptive-field organization of visual neurons in the human brain. This has been our goal for almost a decade, and we have developed methods for doing it in man. These methods are based on the use of microelectrodes developed for implantation in the brains of patients with intractable temporal lobe epilepsy 7 9 The patients in our study were in a group studied by Dr. John E. Adams of the University of California Medical Center in San Francisco. They were to undergo diagnostic and therapeutic brain surgery for relief of their seizures and consented to having the fine microelectrodes added to the usual gross ones. (8,10)

Briefly, the method involves implantation of flexible bundles of eight microelectrodes (Figure 1) in the cortex. Each electrode is made from a 50-u straight tungsten wire etched to a 1-u tip and coated with multiple layers of Isonel 31. They may be included in an indwelling microdrive that can move them from one neural unit to another in the cortex, or they may be left in a fixed cortical locus, in which case electrical pickup of single units is likely because of the large number of active neurons at the tip (Figure 2). (5) The electrodes are introduced through a burrhole 2 cm to one side of the inion. All we can say in identifying the cytoarchitectonic areas is that they are in the visual cortex. It is impossible to distinguish between areas 17, 18, and 19 without histologic confirmation, which we have never had.

FIGURE 1 Microelectrode bundle consisting of eight microtips loosely held together by a small segment of plastic tubing. A separate "ground" lead is deflected to one side. In this model, the tungsten wires are welded to insulated stainless steel leads for greater flexibility and length. The splice is within the Silastic ma ss , which is held firmly in the burrhole by the application of additional Silastic, which forms a plug.

FIGURE 2 Oscillogram recorded from a single unit in the human visual cortex.

Dr. Richard Jung and co-workers(6) first recorded single units in the visual cortex of experimental animals; Hubel and Wiesel(5) and others later demonstrated the receptive-field organization of these cells. The human cortical receptive fields resemble, with some important differences,(8,10) those found in the monkey.(4)

In a series of 15 patients, we observed many units in the visual cortex that did not seem to respond to any stimulus we could provide, whether visual or otherwise. Their "bursty," spontaneous activity appeared independent of external influences. Other units showed a response superimposed on the spontaneous activity when targets were brought within the visual field. This electrical response was amplified until it could be heard over a loudspeaker. With this type of response, we were able to plot nine receptive fields, five in response to disks and the others to bars or lines (Figure 3). The patient fixated a mark on a large sheet of cardboard 1 meter from his eyes. We then moved bars and disks of various sizes and colors and mounted on stiff wire wands within his field of vision and listened for a response. The receptive fields were outlined in pencil on the cardboard for later measurement.

FIGURE 3 Receptive fields recorded from single units in the human visual cortex. See text for explanation.

Because plotting was rapid and could be repeated rapidly, and because the edges of most of the receptive fields were sharp, any wandering of fixation could be detected and thus did not affect the size or position of the plot. Generally, the patients were very cooperative and maintained visual fixation well. Monocular and binocular fields were plotted, and we detected in these patients the various degrees of dominance that have been reported in laboratory animals.

All the receptive fields that we plotted had some characteristics in common. The responses to black on a white background, white on a black or red background, and red, yellow, green, or blue on any contrasting background were equal; the cells were, so to speak, all color-blind.

None of the units or their plotted receptive fields could be influenced by a patient's efforts to change them. For example, we increased the audio gain until the patient could hear the pulses of a unit firing in his cortex and then asked: "Can you hear that? Can you do anything to influence it? Can you increase or decrease it, or affect it in any way?" No matter how much the patient tried to influence the response, we could detect no changes. We also brought the target into the receptive field and asked: "Did you hear that sound when the target was brought here? Now, the target is withdrawn. Imagine it is there and try to make the same sound come from the loudspeaker." No one succeeded in doing that.

None of the units appeared to be influenced by stimuli to other sensory modalities.

All the plotted fields came from excitatory or "on" units, the response being superimposed on the irregular, "bursty" spontaneous rhythm. If there are any inhibitory or "off" units, they appear to be uncommon.

A single unit was usually recordable for the length of a 1- to 2-hr session. At times, a unit would be recordable from one day to the next over the same microelectrode.

The maximal receptive-field response occurred when the target stimulus matched the size and shape of the field. This simple method of target presentation would not be expected to elicit the response of a weak inhibitory surround, and, in fact, we could find no evidence of such a response.

One aspect of our work has direct bearing on the plasticity of the brain, a subject basic to the interests of this conference. Some units showed a progressive attenuation(3) or habitation(2) in their response to repeated stimulation in their receptive fields, which lasted longer than the minute or two reported for laboratory animals. The phenomenon was cortical, in that habituation of a binocular unit by the stimulation of the receptive field of one eye caused a decrement of response in the receptive field of the other eye. A new, nonmonotonous stimulus, either to vision or to another sensory modality, did not restore the response— i.e., did not produce a dishabituation.(1)

The receptive fields are plotted in Figure 3, in which "p" is the fixation point I meter from the eyes. "A" is a receptive field (width, 17 min of arc) of a unit in the ipsilateral or left cortex; the left eye was dominant. All other receptive fields were contralateral to the cortex where their units lay. "B" is a monocular field, right eye, as is "C." "D" is a complex receptive field. Here, a horizontal bar would give a response anywhere within the extent of the field delineated by the horizontal dashed lines. This receptive field also showed marked habituation. "E" is a disk-shaped and "F" is a bar-shaped binocularly equal receptive field; "F" showed marked habituation. "G." "H." and "J" are binocularly equal receptive fields; only "G" showed strong habituation.

Spatial plasticity was also observed in some receptive fields. There appears to be a systematic change with fixation distance of some receptive fields of the angular diameter and the angular position relative to the fixation point. It may involve a size constancy or scaling mechanism. (11,12)

If we are going to investigate plasticity and other subtle functions of the brain, we should, for several reasons, do it in man. First, there appear to be species differences, even between man and monkeys, in receptive-field organization. Second, man not only cooperates with prolonged fixation and specific directed eye movements, but can also be directed to make mental efforts and to describe perceptual responses to stimulation. In this way, the relationship, in terms of unit activity, between simple and complex perceptual tasks, such as reading and its neural basis, can be investigated.

Future developments in neurosurgery may increase the number of potential volunteers for these perceptual-neurophysiologic studies by making unit recording valuable in prognosis and diagnosis of postoperative patients with evacuated hematoma or traumatic encephalopathy. Indwelling microelectrodes that probe the neural organization of the brain should shed more light on the neurophysiologic basis of perceptual disorders.

REFERENCES

1. Horn, G. Neuronal mechanisms of habituation. Nature 215:707-711, 1967.

2. Horn, G., and R. M. Hill. Responsiveness to sensory stimulation of units in the superior colliculus and subjacent tectotegmental regions of the rabbit. Exp. Neurol. 14:199-223, 1966.

3. Hubel, D. H., and T. N. Wiesel. Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. J. Neurophysiol. 28:229289, 1965.

4. Hubel, D. H., and T. N. Wiesel. Receptive fields and functional architecture of monkey striate cortex. J. Physiol. 195:215-243, 1968.

5. Hubel, D. H., and T. N. Wiesel. Receptive fields of single neurons in the cat's striate cortex. J. Physiol. 148:574-591, 1959.

6. Jung, R., R. van Baumgarten, and G. Baumgartner. Mikroableitungen van einzelnen Nenenzellen im optischen Cortex der Katze: die lichtaktivierten BNeurone. Arch. Psychiat. 189:521-539, 1952.

7. Marg, E. A rugged, reliable and sterilizable microelectrode for recording single units from the brain. Nature 202:601-603; 1964,

8. Marg, E. The jigsaw puzzle of visual neurophysiology. First International Conference on Visual Science. Indiana University, Bloomington, 2-4 April 1968. (to be published)

9. Marg, E., and J. E. Adams. Indwelling multiple microelectrodes in the brain. Electroenceph. Clin. Neurophysiol. 23:277-280, 1967.

10. Marg, E., J. E. Adams, and B. Rutkin. Receptive fields of cells in the human visual cortex. Experientia 24:348-350, 1968.

11. Richards, W. Apparent modifiability of receptive fields during accommodation and convergence and a model for size constancy. Neuropsychologia 5:63-72, 1967.

12. Richards, W. Spatial remapping in the primate visual system. Kybernetik 4:146-156,1968.