Contributions to Sensory Physiology: Volume 6

Contributions to Sensory Physiology

William D. Neff

Center for Neural Sciences, Indiana University, Bloomington, Indiana

ISSN  0069-9705

Volume 6 • Number Suppl. (PB) • 1982

Table of Contents

Cover image

Title page

Contributors to This Volume

Copyright page

Contributors

Preface

Contents of Previous Volumes

Volume 1

Volume 2

Volume 3

Volume 4

Volume 5

Cutaneous Communication

Publisher Summary

I Introduction

II The Skin as an Encoding System

III Temporal Relations of Stimuli

IV Pattern Generation and Its recognition by the Skin

Acknowledgments

Effects of Environments on Development in Sensory Systems

Publisher Summary

I Introduction

II. Retrograde and Anterograde Transneuronal Degeneration

III Electrophysiology of Deprived Sensory Systems

IV Binocular Vision and its Critical Period

V Visual Experience and Critical Periods in Avian Species

VI Auditory Stimulation, Plasticity, and Interaural Competition

VII Micro- and Ultramicroscopic Changes

VIII Behavioral Correlates

IX Sensorimotor Coordinations

X Summary and Developmental Principles

Acknowledgments

The Across-Fiber Pattern Theory: An Organizing Principle for Molar Neural Function

Publisher Summary

I Introduction

II Review of the Theory

III Application to Sensory Systems: Sensory Neural Coding

IV Other Processes

V Relation to Several Other Theoretical Statements

VI Concluding Remarks

Acknowledgments

Electrophysiological Analysis of the Echolocation System of Bats

Publisher Summary

I Prelude: Spallanzani’s Bat Problem

II Introduction

III Materials and Methods

IV Emission of Acoustic Signals and Control of Signal Inputs

V Directional Sensitivity of the Echolocation System

VI Processing of Acoustic Signals

Acknowledgments

Coding in the Auditory Cortex

Publisher Summary

I Introduction

II The Basic Auditory Parameters

III Some Anatomical Considerations

IV Tonotopicity

V Feature Detection

VI Auditory Space

VII Transfer

VIII Pitch

IX Cortical Organization

Acknowledgments

The Psychophysics and Physiology of the Lateralization of Transient Stimuli

Publisher Summary

I Introduction

II Stimulus Parameters

III Anatomy

IV Physiology

V Model of Binaural Interaction

Index

Contributors to This Volume

Harvey Babkoff

Robert P. Erickson

Philip H.-S. Jen

Austin H. Riesen

Carl E. Sherrick

I.C. Whitfield

Copyright page

COPYRIGHT © 1982, BY ACADEMIC PRESS, INC.

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Contributors

Numbers in parentheses indicate the pages on which the authors’ contributions begin.

Harvey Babkoff(179),     Department of Psychology, Bar-Ilan University, Ramat-Gan, Israel

Robert P. Erickson(79),     Departments of Psychology and Physiology, Duke University, Durham, North Carolina 27706

Philip H.-S. Jen(111),     Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211

Austin H. Riesen(45),     Department of Psychology, University of California, Riverside, Riverside, California 92502

Carl E. Sherrick(1),     Department of Psychology, Princeton University, Princeton, New Jersey 08544

I.C. Whitfield(159),     Neurocommunications Research Unit, University of Birmingham, Birmingham B15 2TJ, England

Preface

William D. Neff

The publication of Contributions to Sensory Physiology was under-taken with two principal objectives in mind: (1) to bring together reports of current research on all of the sensory systems and (2) to provide an opportunity for the scientist studying a sensory system to give a detailed account of a series of experiments or to present, at some length, a theory about the physiological basis of sensation. It is not the intent of Contributions to present review articles. Authors have been asked to write about their own research findings and theoretical notions and to review the work of others only as it seems suitable for the interpretation of results and theoretical discussion.

Sensory physiology has been given a broad definition—it includes the range from microscopic anatomy to psychophysics. The anatomist has been urged to speculate about the functional significance of his discoveries regarding structure; the psychophysicist has also been encouraged to consider the physiological mechanisms that might explain the findings of his experiments.

It is the hope of the editor and publisher that this serial publication will provide better communication among those who study sensory systems and that it will also be a valuable source of information for scientists from other fields who occasionally seek a representative sample of research that is being done in this important area of physiology rather than just a summary.

Contents of Previous Volumes

Volume 1

CELLULAN PATTERN, NERVE STUCTURES, AND FLUID SPACES OF THE ORGAN OF CORTI

Hans Engström, Harlow W. Ades, and Joseph E. Hawkins, Jr.

FUNCTIONAL ANATOMY OF THE VESTIBULAR AND LATERAL LINE ORGANS

Jan Wersäll and Åke Flock

PSYCHOPHYSIOLOGICAL STUDIES OF VESTIBULAR FUNCTION

Fred E. Guedry, Jr.

BEHAVIORAL AND ELECTROPHYSIOLOGICAL STUDIES OF PRIMATE VISION

Russell L. De Valois

VISION IN INTERMITTENT LIGHT

H. Piéron

AUTHOR INDE—SUBJECT INDEX

Volume 2

THE EVOLUTION OF VERTEBRATE HARING

Willem A. van Bergeijk

THE SENSORY NEOCORTEX

I. T. Diamond

ORGANIZATION OF SOMATIC CENTRAL PROJECTION

D. Albe-Fessard

ELECTRICAL RESPONSES OF THE NERVOUS SYSTEM AND SUBJECTIVE SCALES OF INTENSITY

Burton S. Rosner and William R. Goff

GUSTATORY RESPONSE AS A TEMPERATURE-DEPENDENT PROCESS

Masayasu Sato

AUTHOR INDEX—SUBJECT INDEX

Volume 3

ELECTROPHYSIOLOGY OF VBRATORY PERCEPTION

Wolf D. Keidel

TEMPORAL FEATURES OF INPUT AS CRUCIAL FACTORS IN VISION

S. Howard Bartley

THE MEASUREMENT OF PERCEIVED SIZE AND DISTANCE

Walter C. Gogel

EXPERIMENTAL AND THEORETICAL APPROACHES TO NEURAL PROCESSING IN THE CENTRAL AUDITORY PATHWAY

S. D. Erulkar, P. G. Nelson, and J. S. Bryan

SUSCEPTIBILITY TO ADITORY FATIGUE

W. Dixon Ward

AUTHOR INDEX—SUBJECT INDEX

Volume 4

VISION, AUDITION, AND BEYOND

Frank A. Geldard

PSYCHOPHYSICAL STUDIES OF TMPERATURE SENSITIVITY

Dan R. Kenshalo

PATHOPHYSIOLOGY OF THE FLUID SYSTEMS OF THE INNER EAR

Harold F. Schuknecht

ANATOMICAL ASPECTS OF THE COCHLEAR NUCLEUS AND SUPERIOR OLIVARY COMPLEX

J. M. Harrison and M. L. Feldman

CAT SUPERIOR OLIVE S-SEGMENT CELL DISCHARGE TO TONAL STIMULATION

James C. Boudreau and Chiyeko Tsuchitani

AUTHOR INDEX—SUBJECT INDEX

Volume 5

SIMPLE CELLS OF THE STRIATE CORTEX

G. H. Henry and P. O. Bishop

RELATIONS AND POSSIBLE SIGNIFICANCE OF TASTE BUD CELLS

Raymond G. Murray and Assia Murray

THE NATURE OF TASTE RECEPTOR SITES

Lloyd M. Beidler and Guenter W. Gross

AUDITORY RCEPTOR ORGANS OF REPTILES, BIRDS, AND MAMMALS

Catherine A. Smith and Tomonori Takasaka

OLD AND NEW DATA ON TONE PERCEPTION

Reinier Plomp

AUTHOR INDEX—SUBJECT INDEX

Cutaneous Communication

Carl E. Sherrick,     Department of Psychology, Princeton University, Princeton, New Jersey

Publisher Summary

This chapter provides an overview of skin as an encoding system and the temporal relations of stimuli. It is by now a truism that the mammalian skin is not an insular organ, as are the receptor sites for hearing and vision. What distinguishes the skin from the other major systems is the apparent lack of an ordered geometric configuration of tissues that serves to condition the stimulus energy prior to its impingement on the receptor sites. With respect to temporal summation, it has been shown that the sensitive spots near hairs exhibit this property in the amount of 8 dB to a 20 Hz stimulus—a behavior that is at distinct variance with a hypothesis of a superficial skin receptor that manifests no temporal summation. A recent study of the effects of a masking stimulus on the DL for intensity showed that the DL must be calculated as the increase of intensity, that is, displacement amplitude, above the pedestal provided by both signal and masker. For the skin, the simplest demonstration—conceptually, if not experimentally—requires the presentation of transient pressures of equal sensory magnitude to two separate loci. When the time between the events is varied continuously from 0 to about 1.0 msec, the acute observer perceives only a single tap moving from a central position between the loci toward the site that leads in time of occurrence.

I Introduction

II The Skin as an Encoding System

A Mechanoreceptive Systems in the Skin

B Temporal and Spatial Summation

C The Difference Limen and the Perception of Magnitude Growth

D Sensory Magnitude as a Function of Intensity Levels and Other Variables

E The Effects of Masking

III Temporal Relations of Stimuli

A The Limen for Successiveness of Events

B The Perception of Numerosity

C The Perception of Temporal Order of Events

D Space-Time Interactions on the Skin and Elsewhere

IV Pattern Generation and Its Recognition by the Skin

A Sensory Aids as Tactile Pattern Generators

B A Computer-Controlled Pattern Generator

References

I Introduction

Compared with the senses of vision and hearing, the sense of touch is the autistic child in the family of modalities, for whom the former two constantly interpret to all experimental inquiries. The descriptive qualities of tactile experience are as often as not couched in visual or auditory metaphor, and relayed as speech or as graphic representations of quality or quantity of the experience. It would seem the height of impertinence, therefore, to suggest that touch can reverse the roles and remedy a deficit in hearing or vision, the more so when one of those unfortunate siblings fails after the organism matures.

What the cutaneous sense is being asked to do, however, is not necessarily to assume the full burden ofthe impaired sense, but rather to increase its level of interaction with the remaining senses in such a way that the communicative skills of the individual are brought within the range of social adequacy, as defined by the afflicted person and his or her community. The target for so-called prosthetics research is not the creation of an independent pathway to cognition; it is the development ofa set of interrelations different from thosepreviously in evidence among existing sense modalities. It is, in a Gibsonian (1966) phrase, a reorganization of perceptual systems.

In choosing a course of programmatic research in the area of cutaneous com-munication, we have been faced with the problem of selecting among biases, or emphases, on one or another aspect of the general communication process. One of these is the perceptual bias, which holds that the problem of reorganization rests in great part in the mannerof encoding information for display at the receptor site. A second bias that has had a considerable degree of free play in the past is that the nervous system is sufficiently adaptable so that any display containing the information will eventually be incorporated into the organism’s repertory of meaningful signs through the learning process. Recent modifications of this approach suggest that there may be a critical age beyond which adaptability decreases. Less optimistic students of the problem warn that without the nexus of linguistic competence, as is the case for the prelinguistic deaf child, very little in the way of communicative skill will develop even if a substitute for hearing is provided.

Certain earlier developments in prosthetics research encourage us to believe that the perceptual approach may be fruitful. It has been shown, for example, that some persons are capable of following conversational speech by appropriate placement of their fingers to the lips, jaw, and throat of the speaker. This method, called Tadoma by an American teacher of the deaf (Alcorn, 1945), provides what Durlach et al. (1977) have called an existence theorem in proof of the possibility for tactile communication of speech. In the area of blindness, the skilled use of braill at rates as high as 200 words per minute (wpm) (Gray and Todd, 1968), as well as the regular achievement of rates of reading of 50 wpm by means of the Optacon, a device for translating ordinary print to tactile patterns (Bliss et al., 1970), bear witness to the fact that rapid tactile information processing is a possibility. Thequestions that remain are whether such ratesare the products of virtuoso performances byexceptional persons, or whether judicious modifications of parameters of tactile displays will enable many more handicapped persons to achieve similar levels of skill. The hypothesis proposed by the perceptual approach is that the answer to the latter question is affirmative; furthermore, the learning process should prove to be materially shortened and less arduous if the displays are made compatible with the processing capabilities of the cutaneous system.

II The Skin as an Encoding System

It is by now a truism that the mammalian skin is not an insular organ, as are the receptor sites for hearing and vision. Instead, within the integument, and at various junctures of dermal layers, muscle, ligament, and bone, there are found a variety of free and encapsulated nerve endings to which in the past a great variety of functions have been assigned (see, e.g., Geldard, 1972, p. 275). What distinguishes the skin from the other major systems is the apparent lack of an ordered geometric configuration of tissues that serves to condition the stimulus energy prior to its impingement on the receptor sites. It is clear, nonetheless, that to a rudimentary degree the biophysical analysis of skin and its substrates will yield an elementary form of stimulus organization. Thus far, with a few exceptions, the analysis has barely emerged from the qualitative stage.

A Mechanoreceptive Systems in the Skin

Of the known mechanoreceptive endings, the Pacinian corpuscle is by far the best understood (Loewenstein, 1971). It has, moreover, a wide distribution over the body. At the peripheral level, the Pacinian corpuscle enjoys the services of a single exclusiveaxon, and its response profile is such that a wave of disturbance propagated at some distance from it will excite the attached nervewhen the power involved is as little as 10−7 W (Khanna et al., 1977). This property suggests that a sudden indentation of the skin will evoke a chorus of Pacinian responses from far and near, which while solving the problem of what and when, leaves the question of where to higher levels of the nervous system.

In the course of investigating electrophysiological responses to flutter vibration in monkeys, Merzenich and Harrington (1969) found, besides the Pacinian response profile, a second receptor system. This they identified as alpha quick-adapting afferents, whose loci were near hairs, and whose responses to various frequencies of vibration werequite unlike those of Pacinian afferents, inthat they had a low and broadly tuned sensitivity curve. Spatial tuning of these receptors was, however, exquisite, as von Frey (1915), von Békésy (1939), and Geldard (1940) had shown psychophysically. Merzenich and Harrington noted the same sudden appearance and disappearance of activity as had the previous authors when the vibrating contactor was moved across a sensitive site, suggesting that those traveling waves of pressure, displacement, or shear normally propagated by the skin do not excite such receptors. Indeed, the precise stimulus dimension for excitation is yet in doubt. Geldard (1974) was able to show that extraction of thehair from the follicle lying leeward to the sensitive spot did not affect its vibrotactile threshold, so long as the hair was in the anagenic growth phase. We may deduce from this experiment that, whereas moving the hair does elicit a ready response, the presence or absence of the hair does not bear on the mechanism of excitation when contact with the skin is made directly.

B Temporal and Spatial Summation

Evidence for the integration of activity by these receptor systems over space and time is not univocal. Verrillo (1968) has framed a duplex theory of mechanoreception that hypothesizes two distinctive systems: One system summates energy both temporally and spatially, resulting in a response to vibrotactile stimuli that resembles that of a band-pass filter, having a peak sensitivity near 250 Hz and a 9- to 12-dB per octave slopeon the upper and lower skirts. The receptor is thought to be the Pacinian corpuscle; thesecond system does not summate energy in either space or time, hence, it responds with little variation in threshold over the entirefrequency range, which for prevailing conditions of stimulation ranges from 10 to 700 Hz, or a little over 6 octaves. The receptor identified with this behavior has not been specified. The means for adducing the evidence supporting Verrillo’s hypotheses has been psychophysical, with normal human observers, although the previously cited paper of Merzenich and Harrington, as well as the earlier work by Mountcastle and his colleagues (1967; Talbot et al., 1968) supports the basic premise that at least two receptor systems contribute to the commonly obtained dipper-shaped vibrotactile frequency function.

When similar psychophysical procedures are applied with slightly altered conditions or at sites other than those Verrillo has examined, however, differences in function have emerged. Craig (1968) has shown, for example, that threshold-level spatial summation of separate vibratory inputs can occur in equal amounts whether the sites are ipsilateral or contralateral, suggesting that whatever spatial summation occurs is not peripheral, as Verrillo has hypothesized. Similarly, where suprathreshold stimuli are present,Craig and Sherrick (1969) and Green and Craig(1974) have demonstrated that increasing stimulus area does not effect any more magnitude increase, for a given amplitude of vibration, than does an increase in static contactor pressure without area change. This suggests that the apparent spatial summation, i.e.,increase in perceived magnitude with contactor size, is owing to improved coupling of the driving source to receptor sites (cf. Merzenich and Harrington, 1969, p. 252).

With respect to temporal summation, Geldard (Geldard and Sherrick, 1976) showed that the sensitive spots near hairs exhibit this property in the amount of 8 dB to a 20-Hz stimulus, a behavior that is at distinct variance with Verrillo’s hypothesis ofa superficial skin receptor that manifests no temporal summation (see Fig. 1). It may beobjected that what Geldard was exciting withshort bursts of vibration were Pacinian corpuscles or other distant sites, but that alternative must explain the consistent spatial tuning of the sensitive spot, which, as we have seen, is not a property of Pacinians.

Fig. 1 Temporal summation in vibration-sensitive spots near hairs. Abscissa is the train length, in cycles, of a 20-Hz burst of mechanical vibration. Ordinate is peak-to-peak displacement amplitude required for detection of vibration. Total summation is about 8 dB.

Rollman (1974) was able to show that temporal summation forsingle electrocutaneous pulses, which are assumed to bypass the receptor, is complete for only very brief durations. Between 0.1 and1.0 msec, summation was only partial, and beyond 1.0 msec, no summation occurred. When trains of pulses were presented, however, Rollman found, as had Gibson (1968), that summation occurs for much longer periods. Rollman suggested that the unit-pulse effect is peripheral, whereas the multiple-pulse effect iscentral (1974, p. 43).

C The Difference Limen and the Perception of Magnitude Growth

The manner in which a receptor system encodes energy levels and their variation over time has been the subject of intensive study in the major senses, in great part for the purpose of explaining the complex information-processing capabilities of these systems (Miller, 1956), as well as providing ameans of assessment of degree of loss in deficient systems (see, e.g., Davis and Silverman, 1970). Whereas early studies by Knudsen (1928) suggested a level of intensity and frequency discrimination for vibration that rivaled that of hearing, later studies (e.g., Goff, 1967; Geldard, 1957; Sherrick, 1950) yielded considerably higher values of the difference limen (DL) for both frequency and intensity. The most recent study of the intensitive DL (Craig, 1972) confirms the earlier findings by Geldard and his students (1957) that the relative intensitive DL is about 1.5 dB at high sensation levels, a value that compares poorly with that for the auditory system of 0.25 to 0.5 dB (Sherrick, 1959).

Frequency discrimination in the vibratory domain has been tested from time to time since Knudsen’s early work. Goff (1967) examined the frequency DL for sinusoids from 20 to 200 Hz, andfound relative DLs from 20 to 50%. For pulses, Mowbray and Gebhard (1957) and Franzen and Nordmark (1975) determined values as low as 3 to 6%. More recently, Rothenberg et al. (1977) have reexamined DLs for both types of displacement, and concluded that they decrease from values as high as 50% at 10 Hz to about 10% at 300 Hz. These authors took great care in their psychophysical procedures to provide the observers with a realistic task, as well as in their stimulus control procedures to avoid confounding intensitive changes with frequency shifts.

Of further interest in the experiments of Rothenberg et al. was the finding that quasi-rectangular vibrotactile pulses could be differentiated by observers on the basis of pulse width when frequency of repetition and amplitude were constant. The manner in which the skin encodes this dimension is unclear, but from preliminary observations it seems to be dependent upon changes in pulse rise time (Rothenberg et al., 1977, p. 1006). An early attempt to scale the perception of rise time for sinusoidal bursts was made by Howell (1958), who suggested that what subjects perceive is not rise time, but slope of the signal envelope. By means of information theory analysis, Howell was able to showthat for three or more levels of rise time, the information transmitted was about 1.5 bits. In a later study of the factors affecting perception of rise time, Sheldon (1973) demonstrated that either rise time of the envelope of a sinusoidal vibrotactile stimulus or final intensity level can be manipulated to yield equal magnitudes of sensation growth. Whereas the application of this dimension to working communications systems has not been made, all three of the authors cited havesuggested its potential utility in adding redundancy to tactile codes.

D Sensory Magnitude as a Function of Intensity Levels and Other Variables

Among the earliest studies by Stevens (1959) of the power law was an examination of vibrotactile magnitude, in which the exponent for the usual power law expression was found to be very close to 1.0, with the suggestion that both frequency of vibration and locus of stimulation had some effect on the value of the exponent. In his extensive series of experiments on vibrotactile magnitude functions, Verrillo (1970, 1974; Verrillo and Capraro, 1975; Verrillo and Gescheider, 1976) has been able to show that frequency of vibration does not affect the exponent greatly, but that site of stimulation does. Furthermore, the increase of magnitude with stimulus duration ceases at shorter durations than those given by von Bekesy (1949), whose estimate of duration of growth was 1.0 to 2.0 seconds. Verrillo determined values for growth of 0.6 seconds, in agreement with other recent findings (see Verrillo and Smith, 1976, p. 113).

On the question of magnitude growth with area of the contactor, it is apparent that simple explanations that involve the hypothesis of spatial summation of receptor activities will not serve. Craig and Sherrick (1969) and Green and Craig (1974) were able to show that underlying the summation hypothesis is the premise that the impedance of the skin does not vary significantly over a broad range of frequencies, contactor area, conditions of static contactor force, or presence of static surrounds. So long as displacement amplitude is the exclusive physical measure of stimulus intensity, that premise must be viewed with skepticism.

A departure from the usual measurements of magnitude was made by Craig (1966), who placed separate vibrators at several body loci and, after equating the magnitudes ofeach to a standard 15-dB sensation level (SL) reference vibrator, asked observers to match the total loudness produced when one or more loci were stimulated to that of a single variable vibrator or to the loudness of a variable-intensity, band-limited white noise presented binaurally. The growth of total loudness, i.e., the magnitude ofthe entire pattern with increasing numbers of vibrators, was linear on a log–log plot, with an exponent of 0.46, for matching to a single vibrator. When matching to the auditory signal, the exponent was 0.8, which is predicted from the exponent given above (0.46) divided by the exponent for growth of auditory loudness (0.6). These results indicate that whereas loudness is not summated perfectly among sites to yield an exponent of 1.0, it is summated to a degree, and is independent of site separations greater than a few centimeters as well as of contralateral-ipsilateral distinctions.

In an effort to determine whether the loudness summation function found by Craig applied to a closely spaced set of vibrators, Cholewiak (1979) determined the growth of vibration magnitude on a 64-vibrator matrix. He found that when the number of vibrators, all equal in displacement amplitude, was increased, a doubling of magnitude was reported with each doubling of number. The resulting slope of the growth function is, of course, 1.0, not Craig’s value of circa 0.5. Cholewiak repeated the experiment using several frequencies of vibration, and found lower slopes for 20 and 40 Hz, but beyond these frequencies, uniform values of 1.0 up to 250 Hz were found; moreover, the slope held for different values of display density, i.e., the distance between adjacent active vibrators.

Cholewiak’s finding suggests that, for displays involving varying numbersof vibrators over time, a proportionate reduction of intensity of the active vibrators should occur when the numbers of active vibrators increase. This reciprocal adjustment will help to reduce the possibility of excessive magnitude shifts (producing the haptic equivalent of glare), as well asof masking effects among otherwise unequallyintense successive patterns.

E The Effects of Masking

Early studies of interactions amongmultiple vibrotactile inputs were not oriented to practical applications so much as to comparisons with the auditory system (e.g., Sherrick, 1960, 1964). When the problem of application became apparent, Gilson (1969a,b) examined the effects of placement and number of stimuli on threshold elevation of selected test sites for vibrotactile stimuli. He found that the differential masking effects across body loci could in part be explained by neural delays resulting from unequal distances to the CNS. In addition, Gilson could show that the masking effect of a given number of vibrators was predictable from