Toward a neurobiology of temporal cognition: Advances and challenges

Current Opinion in Neurobiology

Volumn 7, Issue 2, 1997, Pages 170-184

  Gibbon, John ^a   Malapani, Chara ^c   Dale, Corby L ^b   Gallistel, C R ^d  

^a NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTRANSMITTER;

BASAL GANGLION; CEREBELLUM; COGNITION; CONDITIONING; DEREGULATION; HUMAN; MEMORY; NEUROBIOLOGY; PRIORITY JOURNAL; PSYCHOPHYSICS; REVIEW; TIME PERCEPTION;

EID: 0030989710     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(97)80005-0     Document Type: Article

References (136)

1. Kacelnik A, Bateson M. Risky theories - the effects of variance on foraging decisions. Am Zool. 36:1996;402-434.
2. Moore-Ede MC, Sulzman FM, Fuller CA. The Clocks That TIme Us: Physiology of the Circadian Timing System. 1982;Harvard University Press, Cambridge, MA.
3. Church RM. Properties of the internal clock. Gibbon J, Allan L. Timing and Time Perception. 1984;566-582 New York Academy of Sciences, New York.
4. Gallistel CR. The Organization of Learning. 1990;MIT Press, Cambridge, MA.
5. Aschoff J. Circadian timing. Ann NY Acad Sci. 423:1984;442-468.
6. Weber EH. Annotationes Anatomicae et Physiologicae. 1851;CF Koehler, Lipsiae (Leipsig). Observations (and experimentation) anatomical and physiological.
7. Allan LG, Gibbon J. Human bisection at the geometric mean. Learn Motiv. 22:1991;39-58.
8. Gibbon J. Scalar expectancy theory and Weber's Law in animal timing. Psychol Rev. 84:1977;279-325.
9. Gibbon J. Ubiquity of scalar timing with a Poisson clock. J Math Psychol. 36:1992;283-293.
10. Gibbon J. On the form and location of the psychometric bisection function for time. J Math Psychol. 24:1981;58-87.
11. Gibbon J, Church RM. Sources of variance in an information processing theory of timing. Roitblat HL, Bever TG, Terrace HS. Animal Cognition. 1984;465-488 Lawrence Erlbaum Associates, Hillsdale, NJ.
12. Gibbon J, Church RM, Meck WH. Scalar timing in memory. Gibbon J, Allan L. Timing and Time Perception. 1984;52-77 New York Academy of Sciences, New York.
13. Gibbon J, Church RM. Representation of time. Cognition. 37:1990;23-54.
14. Allan LG. The internal clock revisited. Macar F, Pouthas V, Friedman WJ. Time, Action and Cognition: Towards Bridging the Gap. 1992;191-202 Kluwer Academic, Dordrecht.
15. Treisman M. Temporal discrimination and the indifference interval: implications for a model of the 'internal clock'. Psychol Monogr. 77:1963;1-13.
16. Gibbon J, Church RM, Fairhurst S, Kacelnik A. Scalar expectancy theory and choice between delayed rewards. Psychol Rev. 95:1988;102-114.
17. Gibbon J. Origins of scalar timing. Learn Motiv. 22:1991;3-38.
18. Malapani C, Rakitin BC, Meck WH, Levy R, Deweer B, Dubois B, Agid Y, Gibbon J. Coupled temporal memories in Parkinson's disease: a dopamine-related dysfunction. J Cogn Neurosci. 1997;. in press.
19. Rakitin B, Gibbon J, Penney TB, Hinton SC, Malapani C, Meck WH. The peak-interval procedure and cognitive processing of time in humans. J Exp Psychol. 1997;. in press.
20. Gibbon J, Fairhurst S. Ratio versus difference comparators in choice. J Exp Anal Behav. 62:1994;409-434.
21. Gibbon J, Church RM. Time-left: linear versus logarithmic subjective time. J Exp Psychol [Anim Behav]. 7:1981;87-108.
22. Pavlov IP. edn 1 Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex. 1927/1960;Dover Publications/Oxford University Press, New York.
23. Gibbon J, Balsam P. Speading association in time. Locurto CM, Terrace HS. Autoshaping and Conditioning Theory. 1981;219-253 Academic Press, New York.
24. Rescorla RA, Wagner AR. A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. Black AH, Prokasy RF. Classical Conditioning II: Current Research and Theory. 1972;64-99 Appleton-Century-Crofts, New York.
25. of outstanding interest Grossberg S, Merrill JWL. The hippocampus and cerebellum in adaptively timed learning, recognition, and movement. J Cogn Neurosci. 8:1996;257-277 A well written and comprehensive summary of the adaptive resonance theory (ART), which has been developed over the past several years by Grossberg and colleagues. This architecture includes several subsystems: an attentional subsystem, an orienting subsystem, and a comparison subsystem (a vigilance parameter indexes the degree to which stimulus inputs match remembered prototype). The theory includes a spectral timing component posited in the CA3 region of the hippocampus as well as spectrally timed response outputs in the cerebellum. Timing, in both cases, is based on a population of neural units that react at different rates (spectrum) spanning the relevant temporal range. Concomitant habituation processes damp out irrelevant temporal ranges. Arousal from US sources can adaptively select co-active units, which when aggregated, focus attention during a CS that inhibits orienting responses that would otherwise occur during a delay interval and, in the cerebellar timing network, releases appropriately timed behavior at about the CS - US interspike interval (ISI). Combining hippocampal and cerebellar timing permits account of second-order serial learning. Spectral timing in these networks show something approximating Weber's law. The distribution of appropriately tuned receptors is broader at longer ISI's than at shorter ones. However, it is not yet clear that the rate of increase is sufficient to handle the scalar property in detail.
26. Grossberg S, Schmajuk NA. Neural dynamics of adaptive timing and temporal discrimination during associative learning. Neural Networks. 2:1989;79-102.
27. of outstanding interest Raymond JL, Lisberger SG, Mauk MD. The cerebellum: a neuronal learning machine? Science. 272:1996;1126-1131 A review of cerebellar architecture and circuitry relevant to two conditioned behaviors: the conditioned eye-blink response and the VOR (vestibulo-ocular response). The authors argue that similarities in synaptic plasticity of Purkinje cells induced by climbing fiber activation in these two, very different response systems provide a framework for adaptive timing in the cerebellum. They propose that temporally adaptive learning occurs in the cerebellar cortex, with memory storage in the deep cerebellar nuclei. Appropriately timed CR is modelled as a spatially distributed network representation of the delay between CS (parallel fiber activation) and US (climbing fiber activation) in the cerebellum.
28. Gallistel CR. Classical conditioning as an adaptive specialization: a computational model. Medin DL. The Psychology of Learning and Motivation: Advances in Research and Theory. 28:1992;35-67 Academic Press, New York.
29. Libby ME, Church RM. Timing of avoidance responses by rats. J Exp Anal Behav. 22:1974;513-517.
30. Sidman M. Two temporal parameters of the maintenance of avoidance behavior by the white rat. J Comp Physiol Psychol. 46:1953;253-261.
31. Fetterman JG, Killeen PR. Time discrimination in Columba livia and Homo sapiens. J Exp Psychol [Anim Behav]. 18:1992;80-94.
32. Lejeune H, Wearden JH. The comparative psychology of fixed-interval responding: some quantitative analyses. Learn Motiv. 22:1991;84-111.
33. of outstanding interest Ivry RB, Hazeltine RE. Perception and production of temporal intervals across a range of durations: evidence for a common timing mechanism. J Exp Psychol [Hum Percept Perform]. 21:1995;3-18 Three experiments compare the underlying mechanisms of temporal perception and production in the short time interval (325-550 ms) range. The authors found that, when tasks were equated, perception and reproduction of these durations resulted in similar Weber fractions. One experiment also found similar Weber fraction comparing in-phase with out-of-phase test durations, arguing against entrained oscillator models of clock function. Thus, perception and reproduction access similar internal representations of time. implicating a common interval timing mechanism used to measure and discriminate target intervals in both types of tasks.
34. Wearden J. Temporal generalization in humans. J Exp Psychol. 18:1992;134-144.
35. Grondin S, Ivry RB, Franz E, Perreault L, Metthe L. Markers' influence on the duration discrimination of intermodal intervals. Percept Psychophys. 58:1996;424-433.
36. of outstanding interest Miall C. Models of neural timing. Pastor MA, Artieda J. Time, Internal Clocks and Movement. 1996;69-94 Elsevier Science, Amsterdam, A provocative review and exposition of neural network models for time. Miall analyzes problems and advantages of a variety of encoding mechanisms, with special emphasis on difficulties of most of these with intervals in the many seconds range. He describes two models that can handle longer times. One is his 'beat frequency' or coincidence detector mechanism that encodes synchronous beats from a population of oscillator neurons with slightly varying periods. This mechanism can robustly encode intervals up to about a half minute. A second mechanism described is an integrator of oscillatory pacemaker neurons that also has a broader range. Both mechanisms require a (possibly unrealistic) perfect reset common to many network models, so that several trials for learning a duration can encode the same values. The chapter is unusual in its thoughtful, frank evaluation of the strengths and weaknesses of these and other network models.
37. Treisman M, Faulkner A, Naish PL, Brogan D. The internal clock: evidence for a temporal oscillator underlying time perception with some estimates of its characteristics frequency. Perception. 19:1990;705-743.
38. Gray CM, Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA. 86:1989;1698-1702.
39. Joliot M, Ribary U, Llinas R. Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. Proc Natl Acad Sci USA. 91:1994;1748-1751.
40. Church RM, Broadbent H. Alternative representation of time, number, and rate. Cognition. 37:1990;55-81.
41. Keele SW, Nicoletti R, Ivry RI, Pokorny RA. Mechanisms of perceptual timing: beat-based or interval-based judgments? Psychol Res. 50:1989;251-256.
42. Miall RC. The storge of time intervals using oscillating neurons. Neural Computation. 1:1989;359-371.
43. Buonomano DV, Mauk M. Neural network model of the cerebellum: temporal discrimination and the timing of motor responses. Neural Computation. 6:1994;38-55.
44. Buonomano DV, Merzenich MM. Temporal information transformed into a spatial code by a neural network with realistic properties. Science. 267:1995;1028-1030.
45. Levinthal CF, Tartell RH, Margolin CM, Fishman H. The CS - US interval (ISI) function in rabbit nictitating membrane response conditioning with very long intertrial intervals. Anim Learn Behav. 13:1985;228-232.
46. Fiala JC, Grossberg S, Bullock D. Metabotropic glutamate receptor activation in cerebellar Purkinje cells as substrate for adaptive timing of the classically conditioned eye-blink response. J Neurosci. 16:1996;3760-3774.
47. Wearden JH, Doherty MF. Exploring and developing a connectionist model of animal timing: peak procedure and fixed-interval simulations. J Exp Psychol [Anim Behav]. 21:1995;99-115.
48. Herrnstein RJ. Relative and absolute strength of response as a function of frequency of reinforcement. J Exp Anal Behav. 4:1961;267-272.
49. Gibbon J. Dynamics of time matching: arousal makes better seem worse. Psychonomic Bull Rev. 2:1995;208-215.
50. Mark TA, Gallistel CR. Kinetics of matching. J Exp Psychol [Anim Behav]. 20:1994;79-95.
51. Davison M, McCarthy D. The Matching Law: A Research Review. 1988;Erlbaum, Hillsdale, NJ.
52. Herrnstein RJ. On the law of effect. J Exp Anal Behav. 13:1970;243-266.
53. Brunner D, Kacelnik A, Gibbon J. Memory for inter-reinforcement interval variability and patch departure decisions in the starling, Sturnus vulgaris. Anim Behav. 51:1996;1025-1045.
54. Schneiderman N, Gormezano I. Conditioning of the nicitating membrane of the rabbit as a function of CS - US interval. J Comp Physiol Psychol. 57:1964;188-195.
55. Coleman SR, Gormezano I. Classical conditioning of the rabbit (Oryctolagus cuniculus) nictating membrane response under symmetrical CS - US interval shifts. J Comp Physiol Psychol. 77:1971;447-455.
56. Kehoe EJ, Gormezano I. Effects of trials per session on conditioning of rabbit's nictating membrane response. Bull Psychonomic Soc. 4:1974;434-436.
57. Millenson JR, deVilliers PA. Motivational properties of conditional anxiety. Gilbert MT, Millenson JR. Reinforcement: Behavioral Analyses. 1972;97-128 Academic Press, New York.
58. Kehoe EJ, Napier RM. In the blink of an eye: real-time stimulus factors in delay and trace conditioning of the rabbit's nictitating membrane response. Q J Exp Psychol [B]. 43:1991;257-277.
59. Kehoe EJ, Cool V, Gormezano I. Trace conditioning of the rabbit's nictitating membrane response as a function of CS - US interstimulus interval and trials per session. Learn Motiv. 22:1991;269-290.
60. Hinton SC, Meck WH, MacFall JR. Peak-interval timing in human activates frontal-striatal loops. Neuroimage. 3:1996;224.
61. of special interest Jueptner M, Rijntjes M, Weiller C. Localization of a cerebellar timing process using PET. Neurology. 45:1995;1540-1545 Comparisons of brain activation in a time estimation task relative to a comparable motor task was assayed using positron emission tomography (PET) on six normal healthy subjects. Subjects discriminated between a 200 ms (raise right index finger) or 400 ms (raise right middle finger) interval. The authors found significant increases in the activity of superior portions of the cerebellar cortex and vermis in the time estimation as compared to the control task, concluding that these cerebellar areas are involved in timing in humans. Interestingly, they found that thalamic activation, particularly in the right thalamus, increased 10.27%, the largest of any region over the control condition. This may reflect relay activity of cerebellar output to prefrontal and premotor areas perhaps involved in response selection from the temporal information. Similarly, basal ganglia structures (i.e. putamen and globus palidus) showed increases in timing over the control condition. The role of basal ganglia structures relative to that of the cerebellum is still unclear from these results, but both areas are probably involved in timing.
62. of outstanding interest Ivry RB. The representation of temporal information in perception and motor control. Curr Opin Neurobiol. 6:1996;851-857 An articulate summary of recent contributions that support the roles of the cerebellum and basal ganglia in temporal processing. The data reviewed suggest that durations less than 1 s are under cerebellar control, whereas longer durations are modulated by structures within the basal ganglia and striato-cortical loops. Oscillator and distributed network models of the internal clock are described, with particular emphasis on the flexibility of distributed networks that appear best able to mimic data on cerebellar control of temporal processing in classical conditioning.
63. of special interest Meck WH. Neuroanatomical localization of an internal clock: a functional link between mesolimbic-mesocortical and nigrostriatal dopaminergic systems. Behav Brain Res. 1997; A two-part experiment examines the behavioral effects of caudate/putamen (CPu), substantia nigra (SN), and nucleus accumbens (NAS) lesions in rats on temporal discrimination in peak interval procedures. In experiment 1A, a single target interval (20 s) was trained preoperatively. Postoperatively, responding was flat (no peak time) for both lesion groups. Upon further training. SN-lesioned rats showed some recovery of temporal discrimination. In experiment 1B, two target values were trained (10 s and 60 s) preoperatively with rats that subsequently received neurochemical lesions of the CPu or NAS. Results showed a double dissociation. Rats with CPu lesions retained differential responding to the two reward rates, but with a loss of temporal discrimination. NAS-lesioned rats showed no appreciation of the two reward rates, but maintained discriminability of the target times (peak times remained the same). These findings suggest that the mesolimbic and nigrostriatal dopamine systems play different roles in temporal processing. The CPu and SN, through connections from A9, A10 and ventral tegmental area, may act as the clock system for temporal duration, while the NAS is not critical to duration discrimination but is important for hedonic appreciation of relative reward rate.
64. of special interest Meck WH. Frontal cortex or nucleus basalis magnocellularis lesions, but not hippocampal or medial septal area lesions, occasion the loss of control of the speed of an internal clock. Behav Brain Res. 1997; A study of the role of cholinergic and dopaminergic lesions in the basal forebrain and frontal cortical loops on deficits in the clock and memory functions of temporal processing. Lesions in this system (i.e. nucleus basalis magnocellularis [NBM] and frontal cortex [FC]) are compared with those in the hippocampal colinergic system known to affect temporal memory (i.e., medial septal area [MSA] and fimbria fornix [FFx]). Rats were preoperatively trained on the peak interval (PI) procedure at a 40 s target interval. Postoperatively, rats with MSA and FFx lesions underestimated the target interval, whereas NBM- and FC-lesioned rats overestimated the interval. After post-operative retaining, subjects received dopaminergic antagonists (haloperidol and cholecystokinin) and agonists (methamphetamine and a 'surprise' session, representing an arousal condition) in balanced sessions. A double dissociation was found. Drug and arousal manipulations had no effect on MSA- and FFx-lesioned subjects who exhibited the normal horizontal displacement of the timing function, as did control groups. This displacement was not seen in NBM- and FC-lesioned rats. The author concludes that the basal forebrain dopaminergic system increases or decreases clock speed based on training contexts, whereas hippocampal systems modulate temporal memory.
65. of outstanding interest Meck WH. Neuropharmacology of timing and time perception. Cogn Brain Res. 3:1996;227-242 A definitive review of neuropharmacological data on properties of interval timing, particularly those manipulations dissociating attention, scalar variance, and clock and memory components of informations processing. The author argues that dopaminergic manipulations affect clock function, whereas acetylcholine modulates memory for duration. Lesion studies compliment neuropharmacological investigation implicating structures of the basal ganglia in clock function and higher cortical areas in temporal memory and attention.
66. Spetch ML, Treit D. The effect of D-amphetamine on short-term memory for time in pigeons. Pharmacol Biochem Behav. 21:1984;663-666.
67. Rapp DL, Robbins TW. The effects of D-amphetamine on temporal discrimination in the rat. Psychopharmacology. 51:1976;91-100.
68. Stubbs DA, Thomas JR. Discrimination of stimulus duration and D-amphetamine in pigeons: a psychophysical analysis. Psychopharmacologia. 36:1974;313-322.
69. Gibbon J, Farrell L, Locurto CM, Duncan HJ, Terrace HS. Partial reinforcement in autoshaping with pigeons. Anim Learn Behav. 8:1980;45-59.
70. Pastor MA, Jahanshahi M, Artieda J, Obeso JA. Performance of repetitive wrist movements in Parkinson's disease. Brain. 115:1992;875-891.
71. of outstanding interest O'Boyle DJ, Freeman JS, Cody FWJ. The accuracy and precision of timing of self-paced, repetitive movements in subjects with Parkinson's disease. Brain. 119:1996;51-70 A careful study of patients with Parkinson's disease (PD) and age-matched controls, investigating mean interresponse intervals (IRIs) and their variance associated with continuation tapping. A short time interval (550 ms) was tested in both groups. The authors also employed the Wing and Kristofferson [85] model of variance partitioning of 'motor' and 'clock' variance, contrasting ON and OFF states of PD patients, as well as impaired and unimpaired effector in asymmetrical PD, to normal controls. PD patients generally displayed shorter IRI value than controls while response variance was greater in the ON, OFF and impaired effector conditions. A within-patient comparison of impaired versus unimpaired effectors, and OFF versus ON states, also resulted in greater clock and motor variance for impaired and OFF, respectively. These results support dopaminergic/basal-ganglia involvement in the production of short time intervals, conflicting with an earlier report from Ivry and Keele [74] (but see Keele and Ivry [136]).
72. of special interest Freeman JS, Cody FWJ, O'Boyle DJ, Crauford D, Neary D, Snowden JS. Abnormalities of motor timing in Huntington's disease. Parskinsonism Related Disorders. 2:1996;81-93 Two experiments examine accuracy and variability of Huntington's disease (HD) patients in auditory synchronization and continuation tapping tasks. Experiment 1 contrasted mean rates during both cued and uncued tapping for five intervals (frequencies from 1-5 Hz) and the variability (SD) around tap rates. As compared with an age-matched control group, HD patients exhibited less accurate rates, tapping too slowly at short time intervals and too fast at longer intervals, and significantly more variability in mean tap rate. In experiment 2, performance on continuation trials was analyzed at an interspike interval (ISI) of 550 ms. Using the Wing - Kristofferson partition model [85], total variance (TV) around intertap interval (IRI) was partitioned into clock variance (CV) and motor delay variance (MDV). They found that HD patients tapped at shorter IRIs with increased variability. TV, CV, and MDV were significantly higher than controls. These results are consistent with previous findings in patients with basal ganglia dysfunction, and suggest a role for this structure or its afferent connections to higher cortical areas in timekeeper function.
73. Nagasaki H, Kosaka K, Nakamura R. Disturbances of rhythm formation in patients with hemispheric lesion. Tohoku J Exp Med. 135:1981;231-236.
74. Ivry RB, Keele SW. Timing functions of the cerebellum. J Cogn Neurosci. 1:1989;136-152.
75. Pastor MA, Artieda J, Jahanshahi M, Obeso JA. Time estimation and reproduction is abnormal in Parkinson's disease. Brain. 115:1992;211-225.
76. Malapani C, Rakitin BC, Deweer B, Meck WH, Gibbon J, Pillon B, Defontaines B, Dubois B, Agid Y. Segregation of timing processes within the basal ganglia. International Neuropsychological Society 16th European Conference, Angers, March 1994. 1994;23-24.
77. Nichelli P, Clark K, Hollnagel C, Grafman J. Duration processing after frontal lobe lesions. Ann NY Acad Sci. 769:1995;183-190.
78. Shaw C, Aggleton JP. The ability of amnesic subjects to estimate time intervals. Neuropsychologia. 32:1994;857-873.
79. Ivry RB, Keele SW, Diener HC. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res. 73:1988;167-180.
80. of special interest Nichelli P, Alway D, Grafman J. Perceptual timing in cerebellar degeneration. Neuropsychologia. 34:1996;863-872 Patients with cerebellar degeneration were compared to age-matched controls in temporal discrimination experiments using the bisection procedure and a visual bisection control task (line length). Careful psychophysical analysis included calculation of bisection point (PSE), difference limen (DL) and Weber ratio (DL divided by PSE) in both bisection procedures. The discrimination standards (short - long) were: 100-900 ms, 8-32 s, 100-600 ms and 100-325 ms, and 6-54 mm lines. No effect was seen for the line length task, whereas cerebellar patients showed increased Weber fractions at the longest temporal discrimination (8-32 s), but not a lower ranges. Interestingly, the controls' PSE at 100-900 ms, but not the patients', was at the arithmetic mean, suggesting that the discrimination standards were not difficult (a PSE at the geometric mean is common in human and animal data for difficult discriminations; Allan and Gibbon [7]). In contrast to results with 100-900 ms, the 100-600 ms condition of experiment 2 resulted in impairment, but no impairment was seen at the shortest time discrimination (100-325 ms). The authors conclude that the cerebellum is involved in time perception, at both long and short time ranges (above 300 ms).
81. Artieda J, Pastor MA, Lacruz F, Obeso JA. Temporal discrimination is abnormal in Parkinson's disease. Brain. 115:1992;199-210.
82. Lacruz F, Artieda J, Pastor MA, Obeso JA. The anatomical basis for somaesthetic temporal discrimination in humans. J Neurol Neurosurg Psychiatry. 54:1992;1077-1081.
83. Malapani C, Khati C, Dubois B, Gibbon J. Damage to cerebellar cortex impairs precision of time estimation in the seconds range. Cognitive Neuroscience Society meeting, Boston, March 1997. 1997;45.
84. Wing AM, Kristofferson AB. Response delays and timing of discrete motor responses. Percept Psychophys. 14:1973;5-12.
85. Wing AM, Kristofferson AB. The timing of interresponse intervals. Percept Psychophys. 13:1973;455-460.
86. Olszewski J. The Thalamus of Macaca Mulatta. 1952;Karger, Basel.
87. Perrett S, Ruiz B, Mauk M. Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J Neurosci. 13:1993;1708-1718.
88. Thach WT. On the specific role of the cerebellum in motor learning and cognition: clues from PET activation and lesion studies in man. Behav Brain Sci. 19:1996;411-433.
89. Llinas R, Welsh JP. On the cerebellum and motor learning. Curr Opin Neurobiol. 3:1993;955-958.
90. Hallet M. The role of the cerebellum in motor learning is limited. Behav Brain Sci. 19:1996;453.
91. Getty DJ. Discrimination of short temporal intervals: a comparison of two models. Percept Psychophys. 18:1975;1-8.
92. Hirsh IJ, Monahan CB, Grant KW, Singh PG. Studies in auditory timing. 1. Simple patterns. Percept Psychophys. 47:1990;215-226.
93. Malapani C, Deweer B, Pillon B, Dubois B, Agid Y, Rakitin BC, Penney T, Hinton SC, Gibbon J, Meck WH. Impaired time estimation in Parkinson's disease: a dopamine-related dysfunction. Soc Neurosci Abstr. 19:1993;631.
94. Marmaras N, Vassilakis P, Dounias G. Factors affecting accuracy of producing time intervals. Percept Mot Skills. 80:1995;1043-1056.
95. Zakay D. Relative and absolute duration judgements under prospective and retrospective paradigms. Percept Psychophys. 54:1993;656-664.
96. Casini L, Macar F. Prefrontal slow potetials in temporal compared to nontemporal tasks. J Psychophysiol. 10:1996;252-264.
97. Kristofferson AB. A quantal step function in duration discrimination. Percept Psychophys. 27:1980;300-306.
98. Wing AM, Church RM, Gentner DR. Variability in the timing of responses during repetitive tapping with alternate hands. Psychol Res. 51:1989;28-37.
99. Penney T, Allan L, Meck WH, Gibbon J. Memory mixing in duration bisection. Rosenbaum DA, Collyer CE. Timing of Behavior: Neural, Computational, and Psychological Perspectives. 1997;MIT Press, Cambridge, MA. in press.
100. Wearden JH, McShane B. Interval production as an analogue of the peak procedure: evidence for similarity of human and animal timing processes. Q J Exp Psychol [B]. 40:1988;363-375.
101. Rousseau R, Poirier J, Lemyre L. Duration discrimination of empty time intervals marked by intermodal pulses. Percept Psychophys. 34:1983;541-548.
102. Church RM, Gibbon J. Temporal generalization. J Exp Psychol [Anim Behav]. 8:1982;165-186.
103. Clarke S, Ivry R, Grinband J, Roberts S, Shimizu N. Exploring the domain of the cerebellar timing system. Pastor MA, Artieda J. Time, Internal Clocks and Movement. 1996;257-280 Elsevier Science, Amsterdam.
104. Gibbon J. The structure of subjective time: how time flies. Bower G. The Psychology of Learning and Motivation. 1986;105-135 Academic Press, New York.
105. Mellon R, Leak T, Fairhurst S, Gibbon J. Timing processes in the reinforcement omission effect. Anim Learn Behav. 23:1995;286-296.
106. of outstanding interest Gibbon J, Fairhurst S, Goldberg B. Cooperation, conflict, and compromise between circadian and interval clocks in pigeons. Bradshaw CM, Szabadi E. Time and Behaviour: Psychological and Neurobehavioral Analyses. 1997;Elsevier, London, UK, An extensive study of the temporal properties of food anticipation in pigeons in the hours range, manipulating three putative timing systems: a zeitgeberdriven circadian clock, a dawn-initiated interval clock, and a cued interval clock. Variance in responding during the cue was approximately scalar in the duration being timed. Thus, scalar timing in the hours range was seen, but with higher coefficients of variation. Furthermore, striking compromises between disparate predictions of the three clocks were found when phase changes were probed. These compromises required an averaging of each clock's prediction rather than summation, or mixing, of the prediction of each time keeper. It is concluded that computations at the decision stage of information processing, therefore, are far more complex than have generally been postulated.
107. Church RM, Meck WH, Gibbon J. Application of scalar timing theory to individual trials. J Exp Psychol [Anim Behav]. 20:1994;135-155.
108. Church RM, Deluty HZ. The bisection of temporal intervals. J Exp Psychol [Anim Behav]. 3:1977;216-228.
109. Leak TM, Gibbon J. Simultaneous timing of multiple intervals: implications of the scalar property. J Exp Psychol [Anim Behav]. 21:1995;3-19.
110. Brunner D, Kacelnik A, Gibbon J. Optimal foraging and timing processes in the starling Sturnus vulgaris: effect of intercapture interval. Anim Behav. 44:1992;597-613.
111. Maricq AV, Roberts S, Church RM. Methamphetamine and time estimation. J Exp Psychol [Anim Behav]. 7:1981;18-30.
112. Maricq AV, Church RM. The differential effects of haloperidol and methamphetamine on time estimation in the rat. Psychopharmacology. 79:1983;10-15.
113. Meck WH. Selective adjustment of the speed of the internal clock and memory processes. J Exp Psychol [Anim Behav]. 9:1983;171-201.
114. Meck WH. Affinity for the dopamine D2 receptor predicts neuroleptic potency in decreasing the speed of an internal clock. Pharmacol Behav. 25:1986;1185-1189.
115. Meck WH, Church RM. Nutrients that modify the speed of internal clock and memory storage processes. Behav Neurosci. 101:1987;465-475.
116. McAuley F, Leslie JC. Molecular analyses of the effects of D-amphetamine on fixed-interval schedule performance of rats. J Exp Anal Behav. 45:1986;207-219.
117. Branch MN, Gollub LR. A detailed analysis of the effects of D-amphetamine on behavior under fixed interval schedules. J Exp Anal Behav. 21:1974;519-539.
118. Branch MN. Behavioral pharmacology. Iversen IH, Laffal KA. Experimental Analysis of Behavior. 1991;21-77 Elsevier, New York.
119. Santi A, Weise L, Kuiper D. Amphetamine and memory for event duration in rats and pigeons: disruption of attention to temporal samples rather than changes in the speed of the internal clock. Psychobiology. 23:1995;224-232.
120. Rammsayer T, Gallhofer B. Remoxipride versus haloperidol in healthy volunteers: psychometric performance and subjective tolerance profiles. Int Clin Psychopharmacol. 10:1995;31-37.
121. Zis AP, Fibiger HC, Phillips AG. Reversal by L-dopa of impaired leaning due to destruction of the dopaminergic nigro-neostriatal projection. Science. 185:1974;960-962.
122. Meck WH, Church RC, Wenk GL. Temporal memory in mature and aged rats in sensitive to choline acetyltransferase inhibition. Behav Brain Res. 1997;. in press.
123. Meck WH. Attentional bias between modalities: effect on the internal clock, memory, and decision stages used in animal time discrimination. Ann NY Acad Sci. 423:1984;528-541.
124. Meck WH, Church RM. Cholinergic modulation of the content of temporal memory. Behav Neurosci. 101:1987;457-464.
125. Meck WH, Church RM, Wenk GL, Olton DS. Nucleus basalis magnecellularis and medial septal area lesions differentially impair temporal memory. J Neurosci. 7:1987;3505-3511.
126. Meck WH. Cholinergic function and the internal clock. Behav Pharmacol. 5:1994;27.
127. Shurtleff D, Raslear TG, Genovese RF, Simmons L. Perceptual bisection in rats: the effects of physostigmine, scopolamine and pirenzepine. Physiol Behav. 51:1992;381-390.
128. Olton DS, Meck MW, Church RM. Separation of hippocampal and amygdaloid involvement in temporal memory dysfunctions. Brain Res. 404:1987;180-188.
129. Olton DS, Wenk GL, Church RM, Meck WH. Attention and the frontal cortex as examined by simultaneous temporal processing. Neuropyschologia. 26:1988;307-318.
130. Olton DS. Frontal cortex, timing and memory. Neuropsychologia. 27:1989;121-130.
131. Ornstein RE. On the Experience of Time. 1969;Penguin, Harmondsworth, UK.
132. Santi A, Weise L, Kuiper D. Memory for event duration in rats. Learn Motiv. 26:1995;83-100.
133. Penney TB, Meck WH, Allan LG, Gibbon J. Human temporal bisection: mixed memories for auditory and visual signal durations. Collyer CE, Rosenbaum DA. Timing and Behavior: Neural, Computational, and Psychological Perspectives. 1997;MIT Press, Cambridge, MA. in press.
134. Wing AM, Keele SW, Margolin DI. Motor disorder and the timing of repetitive movements. Gibbon J, Allan L. Timing and Time Perception. 1984;183-192 New York Academy of Sciences, New York.
135. Nichelli P, Vernneri A, Molinari M, Tavani F, Grafman J. Precision and accuracy of subjective time estimation in different memory disorders. Cogn Brain Res. 1:1993;87-93.
136. Keele SW, Ivry RB. Modular analysis of timing in motor skill. Bower G. The Psychology of Learning and Motivation: Advances in Research and Theory. 21:1988;183-228 Academic Press, New York.