Physiological Substrates

Habituation: Physiological Substrates, Volume II, presents research and theory that reflect the fact that habituation has achieved a position of prominence among investigators concerned with the neurobiology of behavior. The current interest appears to have evolved from two previously somewhat separate lines of research which have converged upon a common goal, i.e., the understanding of both the behavioral and physiological bases of habituation. The book contains six chapters and begins with one that compares habituation across invertebrate phyla as well as in various types of surgical preparations, presents a quantitative analysis of habituation, and describes neural correlates of habituation in selected preparations and suggests underlying mechanisms. This is followed by separate chapters on habituation in Gastropoda; the role of the auditory receptor, the auditory nerve, and the first central auditory relay (cochlear nucleus) in auditory habituation; habituation displayed by mammalian visual pathway units; habituation in human averaged evoked potentials; and a dual-process theory of habituation.

• Language: English
• Publisher: Academic Press
• Release date: Oct 22, 2013
• ISBN: 9781483262789

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Index

Chapter 1

Comparative Aspects of Habituation in Invertebrates

E.M. EISENSTEIN and B. PERETZ

Publisher Summary

This chapter reviews a comparative study of habituation across invertebrate phyla as well as in various types of surgical preparations. It describes quantitative analysis of habituation and neural correlates of habituation in selected preparations and also suggests underlying mechanisms. Habituation is considered to be a more elemental form of learning than Pavlovian conditioning. It is defined as a progressive decrease in response amplitude or frequency of occurrence to discrete and repetitive stimuli. Habituation studies involve a change in an innate behavioral response. The neural organization underlying this behavior is considered less complex than that involved in other kinds of learning. The chapter also discusses the mechanisms underlying habituation, which shows plasticity in (a) response decrement to repetitive stimulation, (b) recovery of responsiveness, and (c) retention of the effects of previous tests sessions using the same stimulus. It explains that habituating systems not only show response decrement but recovery of responsiveness. An apparent difference between aneural habituating systems and those which contain some level of neural investment is that the latter display dishabituation.

I. Introduction

II. Habituation in Intact Nervous Systems—Selected Examples

III. Ganglionic Changes with Habituation

IV. Plasticity in the Absence of Central Ganglia

A. Facilitation at Neuromuscular Sites

B. Habituation in Peripheral Structures

V. Habituation in the Absence of a Nervous System—Protozoa

VI. Discussion

References

I Introduction

The change in behavior which we term learning has at least two recognizable temporal factors underlying it: (1) the temporal order of events to be associated or learned and (2) the rate at which stimuli are presented. In Pavlovian conditioning we recognize that the change in response of the organism to the conditioned stimulus (CS) is a function of, among other things, the amount of stimulation [number and intensity of the CS and unconditioned stimulus (UCS)] in a given amount of time as well as the temporal order of the CS with respect to UCS.

Habituation is considered to be a more elemental form of learning than Pavlovian conditioning. It is defined as a progressive decrease in response amplitude or frequency of occurrence to discrete and repetitive stimuli. It is also, as is conditioning, dependent on the total number of stimuli presented per unit time; that is, a loud bell which produces an orienting response in a dog will fail to do so at a faster rate the higher the frequency of stimulus presentation. Habituation studies involve a change in an innate behavioral response. The neural organization underlying this behavior is considered less complex than that involved in other kinds of learning. The aim is to specify the mechanisms involved. The mechanisms underlying habituation shows plasticity in (a) response decrement to repetitive stimulation, (b) recovery of responsiveness, and (c) retention of the effects of previous tests sessions using the same stimulus.

An often less recognized but equally important component in the habituation process is the role of temporal order of stimuli in the response decrement seen. Its role is most clearly seen by the effect on the habituation process of altering the temporal order of the stimuli presented. If, in the intermittent presentation of the loud bell in the previous example, another stimulus (or the same one) is presented out of the previous temporal order, a phenomenon frequently seen is an erasure or loss of the previous state of habituation; that is, the probability of response to the stimulus used for habituation tends to return to its starting level or even exceed it (Groves and Thompson, 1970). This phenomenon is termed dishabituation¹ and is clearly an example of the importance of temporal factors in the habituation process as it is in other kinds of learning (Pumphrey and Rawdon-Smith, 1937; Eisenstein, 1967).

Pavlov (1927) first described behavioral habituation in dogs. (Sherrington, in 1906, reported a waning of the scratch reflex in the spinalized dog.) In his review, Harris (1943) stated that representative animals of all phyla display response decrement to repetitive stimuli.

Until recently little attempt had been made to describe specific properties associated with behavioral habituation. Thompson and Spencer (1966) ascribed nine parameters to behavioral habituation which have been extremely useful in comparing various preparations to a relatively fixed set of criteria (see Table I).

TABLE 1

USEFUL PARAMETERS IN COMPARING VARIOUS PREPARATIONS USEFUL PARAMETERS IN COMPARING VARIOUS PREPARATIONSTO A RELATIVELY FIXED SET OF CRITERIAa

j Wood (1970).

aThompson and Spencer (1966).

bHumphrey (1930)

cKupfermann et al. (1970)

dPinsker et al. (1970)

ePeretz (1970).

fBruner and Kennedy (1970).

gSinger and Eisenstein (1972).

hHarris (1943) and Rushforth (1965).

iKinastowski (1963a,b), and Osborn et al. (In press).

kKey: X, yes; O, no; and —, not known.

A number of preparations, intact and semi-intact, from several phyla are listed in Table I. Interestingly enough, what emerges is that three properties are common to almost all: response decrement, spontaneous recovery, and dishabituation. The exceptions are Spirostomum and Stentor, two protozoans which do not appear to dishabituate. Aneural organisms may not possess this property.

We see then that habituating systems not only show response decrement but recovery of responsiveness. An apparent difference between aneural habituating systems and those which contain some level of neural investment is that the latter display dishabituation. A question to consider is whether a habituating system requires synapses to possess the type of plasticity manifested by rapid recovery of responsiveness (dishabituation)?

This review will address itself to (a) comparing habituation across invertebrate phyla as well as in various types of surgical preparations, (b) quantitative analysis of habituation, and (c) describing neural correlates of habituation in selected preparations and suggesting underlying mechanisms.

II Habituation in Intact Nervous Systems—Selected Examples

Habituation in intact coelenterates has been shown. Rushforth (1965), working with Hydra, demonstrated that these animals contract when shaken. When the amount of mechanical agitation was standardized and delivered intermittently, the percentage of contracting animals gradually diminished over a 6 to 8-hour period. This response decrement was found to last up to 4 hours after training. It was not the result of fatigue since contractions could be evoked by a light stimulus after the animals were habituated by mechanical agitation. Dishabituation has been reported in other coelenterates (Harris, 1943).

The nereid polycheates have been shown capable of habituation of the withdrawal reflex through repetition of mechanical shock, a moving shadow, and sudden increases or decreases in light intensity. They are also capable of shock avoidance training. Thus, Clark (1965) has reported that if the worm is placed at the entrance to a glass tube and is shocked when it crawls through to the other side, it crawls more slowly on successive trials, often reversing in the tube to return to the entrance, and eventually refusing to enter. There is considerable retention for 6 hours but almost no retention after 24 hours.

Early behavioral habituation experiments with mollusks showed that snails retained the effects of visual stimuli for at least 24 hours (Piéron, 1909, 1913) and tactile stimuli for several hours (Humphrey, 1930). Also, the rate of habituation was directly dependent upon stimulus rate and appear to follow an exponential curve with respect to time (Pieron, 1913). Humphrey (1930), studying behavioral habituation in the snail, described four of the nine parameters associated with habituation (Table I). The results also indicated generalization of habituation to other stimuli occurred in snails and probably habituation to the dishabituating stimulus.

More recently in a tethered intact Aplysia at least six parameters have been observed (Pinsker et al., 1970; Kupfermann et al., 1970, see Table I). In other experiments carried out in intact Aplysia, the siphon can be made to habituate to either light or tactile stimulation; also, habituation to one stimulus can be dishabituated by the other (Lukowiak and Jacklet, 1972). Long-term studies on intact Aplysia employing tactile stimulation of the siphon show progressive response decrement over days with spontaneous recovery, to some extent, occurring between sessions (Carew et al., 1972). No differences between intact and semiintact Aplysia preparations with regard to the parameters listed in Table I were reported by Pinsker et al. (1970) and Kupfermann et al. (1970). However, there are differences in level of responsiveness and rate of response decrement between Aplysia gill connected to the central nervous system and after connections are severed (see Fig. 13, Black et al., 1972).

Fig. 13 Aplysia gill habituation in the presence of the central ganglion (PVG) and after its removal. The experimental procedures are the same as those shown in Fig. 6. The responsiveness is less and rate of habituation greater with gill connected to the central ganglion. After removal of PVG, responsiveness returns and progressive decrement is seen. Pinnule withdrawal reflex is not independent of central influence which may be expressed as inhibition in the gill. Responsiveness of pinnule withdrawal 30–80% lower with CNS than without CNS. Representative result, one of 16 preparations. (Black, et al., 1972; Peretz & Howieson, 1973)

The data from studies using gastropod mollusk show three parameters are present, response decrement, response recovery after withholding the stimulus, and response immediate recovery after application of a dishabituating stimulus. A minimum rest of 40 minutes restores the responsiveness, at least to the first stimulus (Pinsker et al., 1970). Full recovery, i.e., no obvious effects of previous stimulus sessions, takes much longer. Piéron (1909) found effects which last for a number of hours with about 10% retention after permitting the snail to rest for 24 hours. The results of Piéron (1909) and those in Aplysia suggest a long-term effect of the sessions—perhaps for days. Molluscan neurons possess mechanisms for long-term retention. Strumwasser (1965) has shown that a single neuron in an isolated ganglion removed from the animal, reflects the light entrainment of the intact animal in its spontaneous electrical activity for at least 48 hours. Such experiments suggest competence in single neurons for retention of entrainment and possibly other forms of behavioral modification.

Arthropods have been used to study both behavioral and electrophysiological correlates of habituation. By using the crayfish escape response, Krasne (1969) and Wine and Krasne (1971) have shown that this behavior habituates. The escape response decrements when stimuli are presented at 1 per 5 minutes. Lateral giant fiber activity appears to be involved, at least in the initial stages of the reflex, with medial giant fiber activity contributing to subsequent movements. Both sensory adaptation and fatigue have been ruled out as being responsible for the response decrement. Though dishabituation has not been demonstrated, spontaneous recovery does occur after several hours. Inhibition has been discounted as one mechanism mediating this response diminution because introduction of picrotoxin does not affect the habituation of the escape behavior (Krasne and Roberts, 1967). Picrotoxin is known to inhibit the action of one known inhibitory neurotransmitter in crustaceans, γ-aminobutyric acid (GABA).

III Ganglionic Changes with Habituation

Electrophysiological studies of habituation often measure progressive decrement in the number of spikes elicited to a repeated stimulus. Horridge et al., (1965), for example, reported that the number of spikes elicited in a higher order neuron in the optic lobe of the locust to a spot of light diminishes rapidly by the third stimulus presentation, and the response returns if the light stimulus is moved to a new area of the eye (Fig. 1).

Fig. 1 Typical responses of a novelty unit of the locust optic lobe to a repeated visual stimulus which is changed to a new location after the third presentation. The stimulus was a flash from a small green light source as shown by the thickening in the trace, at a repetition interval of 5 seconds. There is rapid habituation as shown by the first three traces, whereupon at A the light was moved 10° in the visual field without change in the repetition rate or other features. A response almost identical to that first found now reappears. (Horridge, 1965)

Other characteristics of habituated responses were observed in various units of the locust optic lobe. For example, Horridge reported that habituation of a unit through its ipsilateral input leads to diminished output of the unit when its contralateral input is stimulated (contralateral transfer of habituation). Further, a unit previously habituated to light can be dishabituated to light (i.e., the response to light recovers) by presenting a sound stimulus.

Baxter (1957) studied habituation of the running response in cockroaches to puffs of air delivered to the anal cerci. Hairs on the cerci are sensitive to air movement and the cockroach exhibits rapid locomotion to such stimulation. He restrained adult specimens of Periplaneta americana and delivered puffs of air well above threshold for the startle response and visually observed a decline in motor activity. If 1 second puffs of air are delivered at the rate of six per minute, the roach soon ceases to give the characteristic avoiding motor response and exhibits either quiescence or greatly diminished activity. Recording electrical activity of the giant fibers making contact with the primary cercal nerves in the sixth abdominal ganglion, Baxter found no diminution in the electrical acitivity of these giant fibers to puffs of air, even though there is a decrease in the motor activity of the animal. If it is the giant fiber discharges to more anterior portions of the nerve cord that are responsible for the motor activity to the puffs of air, then these results would suggest that the decrease in motor activity resulted from some type of synaptic change anterior to the cercal giant fiber synapses in the sixth abdominal ganglion (very likely in the metathoracic ganglion). Recovery of the habituated response occurs with 5–15 minutes of rest. Baxter cited preliminary work that indicates habituation may take much longer to occur if the higher brain centers are removed by decapitation.

Pumphrey and Rawdon-Smith (1936, 1937) have studied both cercal nerve discharges and synaptic transmission in the last abdominal ganglion of the cockroach Periplaneta americana using acoustic stimuli. They described the cercus as a primitive hearing organ. Recording from the primary cercal nerve, they noted that the nerve discharges are synchronous with tone stimuli from 50 to 400 Hz. The response is only partially synchronized for stimulus frequencies between 400 and 800 Hz; above 800 Hz the response is asynchronous, but they were still able to get a response up to approximately 3000 Hz. They noted with some surprise that so primitive a hearing organ as the cockroach cercus can reproduce so many of the physiological phenomena associated with the vastly more complex mammalian cochlea (Pumphrey and Rawdon-Smith, 1936; Wozniak et al., 1967).

Figure 2 shows the anatomy of the sixth abdominal ganglion into which the primary cercal nerve enters. As can be seen from this figure, the through fibers mostly run on the same side of the cord as the cercus from which they are derived. These are fibers that originate in the cercus and continue right on through the sixth abdominal ganglion to higher parts of the cord. Giant fibers respond in both connectives from a given cercal input—but there is a greater response on the side ipsilateral to the cercal input (Pumphrey and Rawdon-Smith, 1936).

Fig. 2 Sensory input and motor output pathways of the sixth abdominal ganglion of the cockroach P. Americana. (From Pumphrey and Rawdon-Smith, 1937.)

Pumphrey and Rawdon-Smith (1936) noted that when the preganglionic fibers are subjected to repeated supramaximal electrical stimulation at regular intervals, the postganglionic giant fiber response in the last abdominal ganglion is approximately the same, provided that the stimulating frequency is low. The authors noted, however, that with submaximal stimulation of the cercal nerve there was a decrease in the giant fiber output. Such a response decrease occurs even though it appears that the preganglionic response is the same throughout the stimulating period. They attributed this result to a change in the synapses of the last abdominal ganglion, which they designated as adaptation. The postganglionic response may be brought back in one of three ways: (1) by increasing the number of peripheral fibers stimulated, i.e., raising the stimulus intensity; (2) by increasing the stimulus frequency, without modification of its intensity; or (3) by the interpolation of an extra stimulus into the series (Pumphrey and Rawdon-Smith, 1936). The return of an adapted (habituated) response, particularly by the third way, is known as dishabituation. It can be brought about by an interpolated stimulus that is less intense than the stimuli of the series in which it is inserted. The dishabituated response generally occurs to the stimulus in the regular series immediately following the interpolated one. The stimulus frequency used by these authors was generally in the range of about 25 pulses/second. It is the third way of bringing about the return of the response that is of such great interest when considering how nervous systems encode temporal