On sundials, springs, and atoms

Behavioural Processes 44 (1998) 89 – 99

On sundials, springs, and atoms Michael D. Zeiler * Emory Uni6ersity, Department of Psychology, Atlanta, GA 30322, USA Received 20 March 1998; received in revised form 23 July 1998; accepted 27 July 1998

Abstract The orderly behavior that occurs when animals are required to deal with time requirements suggests the possibility that they have an internal clock that provides information about the duration of events. After discussing questions inherent in the concept of an internal clock and suggesting criteria that such a device should meet if it exists, data are reviewed involving several different types of experimental procedures. Every procedure produced different conclusions about the nature of timing. Such results, together with observations of behavior outside of the laboratory, suggest that an internal clock has not evolved and, furthermore, is not even necessary for animals to display temporal regularities in their behavior or to respond to temporal demands. © 1998 Elsevier Science B.V. All rights reserved. Keywords: Interval timing; Internal clock; Timing procedures; Evolution; Rhythms

1. Introduction That all activity necessarily takes place in time is incontrovertible: everything occurs somewhere in the continuous stream of time. Everything also has temporal properties. All events begin and end, which means that they have a localized duration; some repeat at regular time intervals, which means that they display temporal regularity or periodicity. Time is important enough for us to have invented and continually improved mechanical and electronic devices for measuring the duration and periodicity of events. Because our * Corresponding author. Fax: +1 404 7270372.

behavior also shows temporal regularities, it is possible that we have internal devices that can accomplish the same function. The difference is that external clocks are produced and perfected by humans, but an internal clock had to be fabricated over the course of biological evolution. The universality of time complicates matters for scientists who are interested in studying it. Is time itself important in controlling behavior or is it the events that necessarily occur in time that exert control? If the former is true, animals must have internal clocks to keep track of time. However, if the latter is true, temporal regularities in behavior and apparent sensitivities to time reflect something other than readings from a time-measure-

0376-6357/98/$ - see front matter © 1998 Elsevier Science B.V. All rights reserved. PII: S0376-6357(98)00042-4

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ment device serving as a stimulus in the control of behavior. The function of an external time-keeping device is to provide a general-purpose and sufficiently precise measure of time that is independent of the specific temporal properties of the event being measured. Unless an internal clock had this same property, it would not be very useful as a stimulus in controlling behavior. Biological rhythms do not prove the existence of an internal clock; they are only a shorthand way of saying that the behavior is periodic at roughly fixed time intervals. None of these undeniable cases of temporally regular behavior need involve time per se as the controlling stimulus. Animals eat, drink, sleep, mate, and migrate at fairly regular intervals, but the conformity of behavior to any of these periodicities does not require them to use an internal clock to estimate or judge elapsed time or to estimate when the behavior should or should not occur. Eating is controlled by hunger, drinking by thirst, and sleeping by either growing tired or by nightfall or sunrise. The temporal regularity of these activities can occur because temporally regular events (Zeitgebers) modulate internal physiological systems in the direction of the same periodicity. None of this demands that the animal judge time. Reproductive cycles do not require that the animal judge time any more than does the regularity of their heartbeat; they are under the control of a variety of largely involuntary physiological mechanisms. A male does not have to estimate when a female is in estrus, because she generates stimuli that provide the necessary information about her receptivity. She comes into estrus because of temporally regular hormonal cycles, not because of a behavioral clock indicating that now is the time for ovulation. Migration occurs at regular time intervals, but it is triggered by hormones, not by the animals judgment that it is time to move. Fat deposition in birds is closely coordinated in time with the onset of migration, but that does not depend on the judgment that the appropriate time has come to add fat. Time itself probably is no more a discriminative stimulus for behavior instigated by biological rhythms than it is for the production of high and low tides by the moon and sun. Temporal regularities and periodicities do not imply control by time itself.

Another important case of natural time-related behavior is that of coordinated activity. Little is known about the mechanisms used by hunting animals to chase and catch prey. Wild dogs and other carnivorous predators cut corners and thereby head off their fleeing potential meals. The question is whether this hunting behavior involves time as either a discriminative stimulus or as a differentiated property of running as an operant. The behavior can be described as exquisitely paced, but time perception might have little to do with it. Chasing and heading-off can be attributed to perceived changes in spatial relations rather than by temporal judgment based on either discrimination of time or on time as a property of operant responses. Carr and Wilkie (1997) distinguished three types of timing systems. The first two types are ‘ordinal timing’ and ‘phase timing’. Ordinal timing refers to the order of events (‘this event occurs before, or after, or together with another’). Phase timing refers to biological rhythms, where animals show periodicities that are entrained to environmental events. Because neither phase timing nor ordinal timing requires animals to judge the durations of events, neither requires an internal timekeeping device and so do not bear on the nature of internal clocks. The focus must be on ‘interval timing’, which refers to the animal’s ability to judge the duration of a stimulus or to estimate the time between successive events. The main line of evidence for an internal clock comes from studies of interval timing conducted in behavioral laboratories. Richelle and Lejeune (1980) also recognized the need to distinguish between behavior generated by periodicities typical of the animal’s natural ecological niche and behavior generated by arbitrary durations. Biological rhythms and coordinated predatory actions are species-specific natural forms of behavior. But requiring a pigeon to report whether a given duration was long or short or to emit a sufficiently long interresponse time to obtain food is an arbitrary contrivance of the laboratory. From a biological perspective, the need to conform to such temporal demands could not have been predicted in advance for any member of the species, much less for the species as a

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whole. If animals can cope with such arbitrary temporal demands, it must reflect strategies that evolved to deal with unpredictable situations rather than such inevitable regularities as hunger, thirst, sunrise, sunset, or seasonality. A difference between time perception and space perception is that the latter does not seem to share the need to deal with unpredictability. Perhaps the reason for this is that space perception involves known receptors, whereas time perception does not. Because researchers know the receptors, they have been able to make substantial progress in understanding how space is perceived. So, we now know that visual and auditory localization do not stem from the same neural processes, even though they serve the same function of finding where events are occurring. The internal clock could also be modality specific. However, enough data exist on time perception involving visual and auditory events to warrant the parsimonious assumption of a universal internal clock that underlies the judgment of arbitrary durations whether the experience refers to vision, audition, taste, smell, or touch. Such an internal clock would operate independent of the duration being judged, just as do mechanical or electronic timepieces. An internal clock would operate by measuring durations and using its reading to control behavior by serving as either a conditioned stimulus or as a discriminative stimulus. If evolution designed a clock to allow animals to adapt to arbitrary time intervals, it had no way of knowing what events would have to be timed and what the specific intervals might be. It almost had to produce a general purpose clock. It did not necessarily have to be a system that operates fully automatically in the absence of exposure to arbitrary time requirements. Lashley and Wade (1946) said, ‘‘the ‘dimensions’ of a stimulus are determined by comparison of two or more stimuli and do not exist for the organism until established by differential training.’’ With respect to sensitivity to time, they are suggesting that the reality of time to an animal depends on learning that it is important to them. Later research has largely substantiated Lashley and Wade’s assertion (Terrace, 1966). Mere exposure to a stimulus dimension is not sufficient to generate differential

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responding to it; sensitivity requires at least one instance of differential training. Once that sensitivity has been learned, it could transfer to the durations of new events. Time need not be any different in this respect. No matter whether animals have an unconditioned time sense or whether they activate a latent time sense because of differential reinforcement, a universal timing mechanism leads to the expectation that the laws of time estimation would be similar over a range of specific situations. Existing theories relevant to the timing of arbitrary intervals have not paid much attention to this issue, but rather seem to take for granted that the findings they report and explanations they provide will have generality. Consistency across different situations would be compelling evidence for a universal time processing system driven by an internal clock for dealing with arbitrary time intervals. Not a lot of data are available that could help in resolving these issues. What follows is a summary of research that seems relevant.

2. Experimental data on regularities in timing by non-humans

2.1. Temporal differentiation with different responses An old tradition in animal learning has been for the experimenter to choose the animal to be studied and the particular behavior to be observed on the basis of convenience. In modern research, the preferred animals have been rats and pigeons, and the favorite behavior has been barpressing and keypecking. This tradition has also been exemplified in the study of interval timing. However, other responses have been studied as well. When they have been examined, they led to very different conclusions about the nature of timing than had been drawn from observations of bar-pressing or key-pecking. In what seems to be the first comparison of different responses, Hemmes (1975) required pigeons to space their responses appropriately to obtain food. The response was either key-pecking or treadle-pressing. The pigeons met the spacing

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requirements much better when they had to press the treadle than when they had to peck the key. When Richardson and Clark (1976) followed up on Hemmes’ study, they used a wider range of spacing requirements and ensured that training was continued until the behavior reached steadystate. They found that the average time between successive responses and the number of responses per food delivery increased with longer requirements with both responses. But generality ended there. When it came to temporal control, keypecking revealed considerably more precise timing than did treadle-pressing. Lejeune and Jasselette (1986) extended the study of spaced responding to comparisons between perching responses and treadle-pressing. The pigeons spaced their responses accurately even with the longest spacing requirements when the response was perching, but that did not occur with treadle-pressing. In the case of perching, the average time between responses over much of the range of requirements approximated a linear function. In the case of treadle-pressing, the function was clearly non-linear. It had the characteristics of a power function with an exponent much less than 1.0. As is always the case with fractional exponents, the birds were largely insensitive to longer spacing requirements imposed on their treadle presses. Furthermore, the coefficients of variation—a common measure of temporal sensitivity in experiments imposing temporal requirements on behavior— were minimally doubled for treadle-pressing as compared with perching. Platt (1984), applied timing requirements to four temporal properties of two different responses (a 4×2 design). The properties were response latency, the time between successive responses, the time to change from one response to another, and the duration of the response. The two responses were lever-pressing and extending the snout into an opening in the ceiling of the experimental chamber. The particular response used produced differences in the timing of each temporal property, and the four temporal properties differed from each other. Once again, conclusions about timing differed depending on the response that had to be timed.

2.2. Comparisons of temporal differentiation and temporal discrimination Experiments using fixed-ratio schedules showed that if the time taken to begin and to complete the sequence had to conform to a criterion, pigeons changed their sequence durations in the appropriate direction (Zeiler, 1970, 1972; DeCasper and Zeiler, 1977, 1974). The orderly effects of this temporal differentiation procedure were on overall duration, not on any smaller component such as the initial pause or the time spent responding after the pause. The theoretical paper of Gibbon (1977) on scalar timing theory asserted that scaling of time is linear. Linearity means an exponent of 1.0 when durations produced by the animal are considered as power functions of the standard. An experiment on differential reinforcement of single bar-press durations by rats (Platt et al., 1973) had revealed exponents around 0.9, and one on differential reinforcement of response latency in pigeons (Catania, 1970) had shown exponents around 0.8. Gibbon suggested that since the only information an animal has about time requirements comes from the durations that are reinforced, they must provide the standard for the animal. When he substituted the durations actually followed by reinforcement for the time requirement, the exponents for the Platt, et al., data became 1.0. He was not as successful with Catania’s latency experiment. The data on fixed-ratio sequence durations did not fit. The exponents relating fixed-ratio sequence duration to the reference time standard remained between 0.6 and 0.8 even when the standard was taken to be reinforced duration, and they were slightly smaller when the standard was assumed to be the duration requirement that had to be met for the pigeons to get food. These various results meant that although temporal differentiation of single bar-press durations by rats supported linear scaling, differentiation of both response latencies and fixed-ratio sequence durations by pigeons did not fit the same conclusions. That it was not a species difference was evident when linear timing did occur with pigeons if the situation was changed to eliminate the need for a response after the reference time had elapsed

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(Zeiler, 1985). Also, an experiment on differential reinforcement of pigeon peck duration showed exponents of B0.43 with respect to required duration and of about 0.5 with respect to reinforced duration (Zeiler et al., 1980). Note that the departure from linearity with single responses could have been due to short latency autoshaped responses interwoven with those that were timed, but that is implausible in the case of fixed- ratio sequences involving 15, 30, or more responses. Gibbon (1977) also argued that the extant data supported the assertion of scalar theory that Weber’s law fit timing, which had been asserted previously by Stubbs (1968) and Catania (1970). The experiments on fixed-ratio sequences, like those on single response latencies and single barpress durations, seemed to agree. However, the work of Cantor (1981) showed that not all animal timing results fit Weber’s law. A review of the temporal differentiation data revealed that eyeball fits to Weber’s law did not survive quantitative analyses either (Zeiler, 1986). Instead, of being constant as per Weber’s law or decreasing as per the generalized form (Getty, 1975) of the law, Weber fractions usually rose with longer duration requirements.

2.3. Temporal reproduction In an attempt to provide pigeons with unambiguous information about the time requirement, Zeiler and Hoyert (1989) presented pigeons with a stimulus of a certain duration. The pigeons then received food if their minimum time for beginning and completing a sequence of 15 responses matched or exceeded the signal duration by no more than 50%. The number of different signals presented ranged from one to ten in different conditions. The mean sequence durations emitted were described equally well as linear or power functions of signal duration, with the mean interresponse time consistently underestimating the signal duration. All four birds revealed increasing coefficients of variation with longer signal duration when the procedure involved four or fewer signals. With six or more signals, two of the birds developed constant coefficients as predicted by Weber’s law, but the other two continued to show

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increases with longer signals. There were clear differences in performance among the four birds as the number of signals increased, which suggests that the birds were dealing with the situation in different ways.

2.4. Temporal bisection Temporal bisection experiments are intended to discover the duration that the animal treats as midway between two or more standard durations. In a discrimination version, Church and Deluty (1977) presented rats with two durations. Which lever was correct depended on whether the stimulus duration was the shorter or the longer one. Intermediate probe durations allowed determination of the value that produced equal responding to the two levers. Other discrimination versions of the procedure (Stubbs, 1968) involved ten stimulus durations. The defining attribute of a discrimination procedure is that the animal is presented with a stimulus for some duration and then must classify it with a non-temporally-defined response. The differentiation version of the bisection procedure requires that the animal time its response. For example, Stubbs (1980) arranged for food delivery to occur at one of ten durations following the onset of each trial. The response key was orange at the start of the trial, and it changed to green only if and when the pigeon pecked a second key. Food delivery occurred when the pigeon pecked the response key at the time since trial onset that food was available. However, for the five shortest assigned durations, the response key had to be red for a response to produce food; for the longer durations, it had to be green. The critical measure for the differentiation version of bisection was when on each trial the pigeon changed the response key color from orange to green. The power mean is a sensitive measure of the bisection point. Each duration is raised to the same power (a), and the average of these values is calculated. The exponent a is iterated until the average taken to the 1/a power corresponds to the bisection point obtained in the experiment. If the arithmetic mean describes the data, the exponent will be +1.0; if the harmonic mean applies, the

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exponent will be −1.0; if the geometric mean is best, the exponent has a small value near 0.0. The majority of discrimination procedures yielded strongly positive exponents, but the differentiation procedures yielded strongly negative exponents. Once again discrimination and differentiation procedures led to different conclusions about the properties of an internal clock.

2.5. Temporal discrimination Most experiments on animal timing have involved temporal discrimination rather than temporal differentiation. In temporal discrimination, the animal does not produce the relevant duration, but instead evaluates the duration of stimuli previously presented by the experimenter. The temporal reproduction experiment (Zeiler and Hoyert, 1989) added a prior potential temporal discriminative stimulus to a differentiation procedure. All of the discrimination data appeared to fit some form of Weber’s law, and the few that also provided information about scaling implied linearity. These results suggested that even if timing is not scalar when animals must produce behavior having a certain duration, it is scalar when they must judge the duration of a past external event. The implication is different timing processes for discrimination and for differentiation. The scalar property did appear in differentiation with the reproduction procedure. Yet even there differences emerged on closer examination of the linear functions. Discrimination procedures typically have generated linear functions with coefficients \ 1.0 (consistent overestimation of stimulus duration), whereas those fit to the temporal reproduction data had coefficients B1.0 (persistent underestimation of stimulus duration).

2.6. Timing in open and closed feeding economies The commonly used experimental procedures, including the ones described above, were similar in several regards. Most involved food as the reinforcer for food-deprived animals who received supplementary feeding outside of the experiment in order to maintain them at some predetermined percentage of their free-feeding weights. They also

provided the animals with brief accesses to food during the experiment. Collier’s (Collier, 1983) multiple demonstrations that schedule behavior differed enormously depending on whether animals were food-deprived, got small amounts of food at each opportunity, and received supplementary meals or had a different regimen where they were not deprived, ate all they wanted at each opportunity, and had no supplementary feeding. This provided another vehicle for studying constancy in timing processes. Two studies were conducted on timing in both kinds of feeding situations. In one experiment (Zeiler, 1991) pigeons in an open economy were maintained at 80% of their free-feeding weights, had a brief food delivery for each correct timing, and got post-session food supplements as needed. In the closed economy, they were not food-deprived, they ate freely when they timed correctly, and they ate only what they earned. The first experiment was on temporal discrimination. The procedure was borrowed from that of Church et al. (1976) to determine rats’ sensitivity to differences in stimulus duration. Either a short or a long duration stimulus occurred on each trial. To obtain food, the pigeon had to peck one key if the duration had been the short one and a different key if it had been the long one. Correct responses to the long duration made it shorter on the next trial, incorrect responses made it longer. The logic of this titration or staircase procedure is that as long as the bird can discriminate between the two durations, it should respond correctly to both. This means that the long duration eventually has to become indistinguishable from the short, and the animal then will respond to it as if it was the short one. These errors drive the long duration up until it becomes long enough to once more be discriminably different. The long duration should oscillate around the difference threshold. Nine short standard durations ranged from 0.25 to 64 s in both open and closed economies. The data for the two economies were opposites of each other. In the open economy the Weber fractions rose from 0.2 to 0.7 with longer standards. In the closed economy they decreased from 0.9 to 0.3. The rising curves for the open economy fit no

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form of Weber’s law. The falling curves for the closed economy corresponded somewhat to the generalized form of Weber’s law. Most important was that how pigeons timed in the same discrimination problem varied in fundamental and nontrivial ways with the feeding economy. An accompanying temporal differentiation experiment required pigeons to space their responses to get food. Seven interresponse time (IRT) requirements had lower bounds from 0.5 to 32 s. The bird initiated the relevant time interval. Data were collected separately for first responses (those preceded by a food delivery) and for subsequent responses (those following an incorrectly spaced response). For first responses, exponents relating mean IRT to either the lower bound or mean reinforced IRT averaged 0.79 in the open economy and 0.23 in the closed. For subsequent responses, exponents were 0.57 in the open economy and 0.74 in the closed. Timing varied with feeding system and with which pecks were considered. Weber fractions showed differences as well. First-response coefficients of variation rose with longer requirements in the open economy, but not in the closed. For responses following the first, coefficients increased in the open economy but decreased in the closed. Once again the open and closed economies suggested different timing processes under experimental conditions that were otherwise the same. The results reported to here indicate that temporal differentiation and temporal discrimination typically resulted in different pictures of the nature of time estimation even in the same feeding economy. Furthermore, the same discrimination or differentiation problems produced different timing depending on the feeding economy. Consistent timing data were becoming ever more problematic.

2.7. The peak procedure The peak procedure was invented by Catania (1970) and became widely known after its use by Roberts (1981). In most trials food is delivered according to a fixed-interval (FI) schedule. In the rest food is omitted and the trial continues much longer. The idea is that where response rate peaks

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on these empty trials measures timing of the moment of reinforcement. Even an ordinary FI schedule reveals how the time parameter controls when responding begins or when response rate maximally accelerates. Empty trials add the ability to see when responding stops or maximally decelerates. Zeiler and Powell (1994) used the peak procedure with seven fixed intervals ranging from 7.5 to 480 s. The results were analyzed in terms of when responding began in each interval, when it maximally accelerated, when it maximally decelerated, and when it stopped on each empty trial. The analysis included the now-conventional calculation of statistical peak points even though a discrete peak rarely occurred on any empty trial (Gibbon and Church, 1990). Every measure yielded unique conclusions. For initial pauses power function exponents were close to 1.0, and coefficients of variation rose with longer FIs. For points of maximum acceleration exponents were around 1.0, but now coefficients of variation varied randomly. Stopping time was moot, because the birds usually responded throughout an empty trial. Points of maximum deceleration were fit by exponents greater than 1.0, but coefficients of variation fell with longer FIs. Peak points had exponents of about 1.1, and coefficients of variation increased with longer FIs. These results fit with those on temporal differentiation of different responses reported by Platt (1984). Whether the procedure involved explicit differential reinforcement (Platt) or not (peak procedure), conclusions about timing varied with the behavior presumably being timed.

3. Discussion The data confirm the many other observations from numerous laboratories showing unambiguously that animals are able to cope with a variety of experimental demands involving arbitrary duration requirements. However, the data also indicated that the principles of behavioral timing varied with the particulars of the situation. Such observations do not support the concept that the solution to timing problems involve the same

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processes or a common internal clock that underlies the ability to discriminate the duration of external events or of ongoing behavior. How are these various data to be understood? An equation with enough fitting parameters and no constraints on their values surely could do the job, but that would only testify to the power of curve-fitting. The challenging problem is to understand why the way that animals time arbitrary events depends on the particulars of the time requirements and the procedure under which they are imposed. An important step in understanding biological systems is to determine what they accomplish for the organism. Why does anyone need to judge time? Sensitivity to time clearly matters for humans who must get to meetings, pick up children, and meet deadlines. The need to conform to social conventions provides enough history of differential reinforcement with respect to time to activate a time sense. ‘‘Without [a common language of time measurement] and without general access to instruments accurate enough to provide uniform indications of location in time, urban life and civilization as we know it would be impossible. Just about everything we do depends in some way on going and coming, meeting and parting’’ (Landes, 1983, p. 2). Nothing that Landes has said requires humans to have an internal timing system; it explains only why people had a strong need for external clocks. Because of their need to deal with time, humans have developed and used a number of devices for discriminating appropriate time periods. Examples of invented discriminative stimuli include calendars to deal with years, months, and days and watches or clocks to deal with hours, minutes, and seconds. Astronomers, who may have been the first needing to differentiate short time intervals, demanded appropriate mechanical devices, because their inherent skills were insufficient. Athletic activities need to be timed in short intervals, but this cannot be done adequately without mechanical or electronic timers. Cooks preparing familiar recipes still depend on external clocks, or on smells and tastes. If even humans with a long history that has emphasized the importance of time still need so much external mechanical support, the possibility arises that maybe most hu-

mans do not possess an internal clock for measuring duration. That hypothesis fits the observation that when humans must estimate time without external help they so often resort to counting. The absence of an internal clock for arbitrary durations also explains why humans depend so much on visual or auditory guidance instead of on their own ability to deal with time. Non-humans are even more problematic, because they may never need to deal with arbitrary time at all before they are brought into a laboratory. Even those animals that are social have no apparent need to schedule their days in the way that humans do. Not even non-human primates seem to arrange meetings at a specific time or to impose deadlines on themselves or on others. Either internal or external stimuli guide their behavior well enough to obviate the need for of a sense of time. Eat when hungry, sleep when tired or when it gets dark, wake when it gets light or the alarm goes off, mate when sexually aroused and the potential mate displays the appropriate external stimuli. These events mitigate the need for actively estimating how much time has passed. What important difference does it make for an animal to know how long ago something happened or how long a particular behavior pattern has been going on independent of the observable stimuli that are present? Social training can provide the necessary history for humans to make them aware of time, but it is not obvious that it serves the same role for non-human animals. They may become aware of time only given some other kind of differential reinforcement with respect to duration. That may happen rarely if ever in the animal’s natural environment. If so, animals may actually not learn about time until an experimenter gives them differential reinforcement based on the duration of stimuli or on a temporal property of their behavior. It is then that the animal first becomes sensitive to the duration of events. However, human experience suggests that despite a history of differential reinforcement, few people ever get good enough at estimating time for the sensitivity to be useful. Non-humans in the laboratory are similar. Even after months of differential training with time requirements, rats and pigeons continue to

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do quite poorly, particularly in temporal differentiation problems. Standard deviations of emitted durations are often 30% of the mean or more, and emitted durations can differ from required durations by 50% or more. Even after years of exposure to the same fixed-interval schedule animals continue to start responding long before the interval elapses. The initial pause typically ends no more than 50–60% into the interval, and the pause times remain highly variable. Such enormous variability and stubborn inaccuracy suggest that animals are no better than humans at estimating time. If they do develop sensitivity to time following differential reinforcement and they then activate a time sense that they can use to estimate durations, why is it that most continue to depend on other more accessible cues that may be around? In the absence of watches, people do not measure time all that well. Other animals also time perfectly when given analogues of the external clocks that made time discrimination irrelevant in their evolutionary history. But without them they never are accurate time-keepers. When deprived of external support and left to rely on time estimation, as they are in the experiments reviewed earlier, animals rarely cope very well. Furthermore, even when they do cope, they are likely to do it differently in different situations. Not all biological mechanisms evolved because they were useful; contemporary evolutionary theorists recognize the importance of processes other than natural selection. The present suggestion is that an internal behavioral clock for dealing with arbitrary time intervals never evolved at all. The lack may be because mechanisms for judging time directly may never have existed to be selected by evolutionary forces. Or, it might be that even if an incipient internal clock appeared, it might not have been subject to selective pressure for continued existence and refinement because it imposed a physiological house-keeping burden without offering any advantage over dependence on other events. The present hypothesis can be viewed as another instance of the idea that timing in laboratory settings that preclude correlated visual, auditory, olfactory, or tactual stimuli is carried by non-timed responses [see Richelle and Lejeune

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(1980), for an excellent review]. It also makes limited contact with contemporary timing theory, in particular one aspect of the behavioral theory of timing (Killeen and Fetterman, 1988). According to this theory, which accounts for a large amount of experimental timing data, animals make transitions between classes of adjunctive responses. Pulses from an internal generator cause the transitions. The adjunctive behaviors come to serve as discriminative stimuli for other responses. The clock pulses themselves are not discriminative stimuli, because they are indistinguishable from each other; the animal does not count pulses, but instead is driven from one adjunctive state to the next. From the present perspective, adjunctive behavior elicited by the reinforcing stimulus and other experimental stimuli is a reasonable candidate for the behavior that is invoked in timing experiments. If the mediating behavior was random, one might expect larger individual differences in behavior than have actually occurred in studies of timing that focused on the behavior of individual animals. Adjunctive behavior produced by particular situational stimuli restricts the possibilities and thereby might result in similarity among the different animals in any given experiment or set of experiments. The occurrence of sequences of different types of adjunctive behavior also helps in understanding why performance persists in being highly variable in these experiments. External guidance seems to be the only way for humans and other animals to be temporally precise. Another possibility avoids the postulation of unseen adjunctive behavior as the source of temporal control in arbitrary interval timing in the absence of external supporting stimuli. It would be time-based than behavior-based. Animals confronted with arbitrary timing problems might draw on the same oscillators that underlie their biological rhythms. Which ones they use would be likely to depend on situational specifics, but they might be similar across members of a given species. If the oscillators vary in their periodicity, the timing behavior would change in different situations. How these oscillators might translate into the control of observable behavior in the absence of correlated external stimuli remains to be dis-

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covered (some form of counting might be involved). An appeal of this possibility is that it might not entail the multiplicity of interacting factors that characterize contemporary theories of interval timing. The tentative conclusion is that neither humans nor any other animals deal with arbitrary durations as they should if they have a general-purpose internal clock. Yet they do cope better with arbitrary durations after training than they did at the outset. Extrapolation from the various observations proposed above suggests that instead of using one timing mechanism, animals come to depend on some time-correlated behavior or some chance or consistent stimulus that seems to help it get food or avoid shock now. The sources of control keep shifting as experimenters revise what they ask the animal to time and the animals struggle to adapt to the particular demands of their current ecosystem. If we want to maintain that internal clocks for timing arbitrary intervals exist, we may need to accept that there are many, and they may work in very different ways. It is as if the nature of the clock changes with every alteration in what animals are required to time. The clocks invented by people over the course of human civilization have taken manifold forms, and the same would have to be true of those invented by nature. But then finding out how one clock works would tell us nothing about another. Sundials tell us little about grandfather’s clocks, and spring-driven wristwatches do not help us understand how electronic timepieces work. Equally radical discontinuities may also be true of the many internal clocks that might come into play when animals must cope with arbitrary time intervals. Why nature has tolerated such inefficiency need not be a mystery. It would follow if interval timing per se never evolved, either because it never existed to be selected or because it helped little or not at all in solving survival problems. Laboratories do not necessarily model the problems posed by nature. The intention is not to reject the existence of any kind of general-purpose internal timing mechanism. In fact, there is strong evidence that animals are sufficiently sensitive to at least one temporal aspect of their environment as to suggest

the existence of one kind of internal timing mechanism. Without any apparent need for training, humans (and perhaps non-human animals as well) keep time with music and are sensitive to rhythms in speech and other environmental events. Humans also utilize rhythms to keep track of time, as when they say ‘‘one one-thousand, two one-thousand’’ and so forth. Something must underlie such a pervasive sense of rhythm. The driving force could be the same pacemakers that drive the biological rhythms that can be so readily entrained to environmental regularities. These pulses probably are indistinguishable from those proposed by the behavioral theory of timing as the cause of transitions in adjunctive behavior. In fact, the paced counting mechanisms so commonly used by humans follow from that theory. Perhaps rhythmicity stems from the matching of external events to the beating of such clocks. Humans have devised many devices for recording time. Sundials worked to some extent in fair weather, but they never matched the utility of spring-driven pocket watches. Eventually quartz crystals and atomic vibrators allowed unprecedented levels of accuracy at amazingly low cost. But biological evolution has never matched cultural evolution in the manufacture of clocks. Nature granted animals only inherently variable biological metronomes and the ability to use them in flexible ways. Anything better was the outcome of making humans such highly social animals that they needed to covet, invent, and produce evermore accurate instruments for communicating their experiences and coordinating their activities with others.

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