The neural basis of temporal auditory discrimination

When two identical stimuli, such as a pair of clicks, are presented with a sufficiently long time-interval between them they are readily perceived as two separate events. However, as they are presented progressively closer together, there comes a point when the two separate stimuli are perceived as one. This phenomenon applies not only to hearing but also to other sensory modalities. Damage to the basal ganglia disturbs this type of temporal discrimination irrespective of sensory modality, suggesting a multimodal process is involved. Our aim was to study the neural substrate of auditory temporal discrimination in healthy subjects and to compare it with structures previously associated with analogous tactile temporal discrimination. During fMRI scanning, paired-clicks separated by variable inter-stimulus intervals (1-50 ms) were delivered binaurally, with different intensities delivered to each ear, yielding a lateralised auditory percept. Subjects were required (a) to report whether they heard one or two stimuli (TD: temporal discrimination); or (b) to report whether the stimuli were located on the right or left side of the head mid-line (SD: spatial discrimination); or (c) simply to detect the presence of an auditory stimulus (control task). Our results showed that both types of auditory discrimination (TD and SD) compared to simple detection activated a network of brain areas including regions of prefrontal cortex and basal ganglia. Critically, two clusters in pre-SMA and the anterior cingulate cortex were specifically activated by TD. Furthermore, these clusters overlap with regions activated for similar judgments in the tactile modality suggesting that they fulfill a multimodal function in the temporal processing of sensory events.

[1]  T. Rammsayer,et al.  Effects of Noradrenergic Activity on Temporal Information processing in Humans , 2001, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[2]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[3]  Christian Gaser,et al.  Processing of temporal information and the basal ganglia: new evidence from fMRI , 2003, Experimental Brain Research.

[4]  Laura Bertolasi,et al.  Timing of tactile and visuo-tactile events is impaired in patients with cervical dystonia , 2004, Journal of Neurology.

[5]  H P Ludin,et al.  Impaired somatosensory discrimination of shape in Parkinson's disease: Association with caudate nucleus dopaminergic function , 1999, Human brain mapping.

[6]  R. Miall,et al.  Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging , 2003, Current Opinion in Neurobiology.

[7]  S Lehéricy,et al.  Basal ganglia and supplementary motor area subtend duration perception: an fMRI study , 2003, NeuroImage.

[8]  Karl J. Friston,et al.  The Functional Neuroanatomy of Temporal Discrimination , 2004, The Journal of Neuroscience.

[9]  F. Vidal,et al.  Activation of the supplementary motor area and of attentional networks during temporal processing , 2002, Experimental Brain Research.

[10]  J M Dambrosia,et al.  Abnormalities of spatial discrimination in focal and generalized dystonia. , 2003, Brain : a journal of neurology.

[11]  A. Ferrandez,et al.  ERPs and PET analysis of time perception: Spatial and temporal brain mapping during visual discrimination tasks , 2000, Human brain mapping.

[12]  W. Meck,et al.  Dissecting the Brain's Internal Clock: How Frontal–Striatal Circuitry Keeps Time and Shifts Attention , 2002, Brain and Cognition.

[13]  R. E. Passingham,et al.  Changes in the Human Brain during Rhythm Learning , 2001, Journal of Cognitive Neuroscience.

[14]  P. Maquet,et al.  The basic pattern of activation in motor and sensory temporal tasks: positron emission tomography data , 1997, Neuroscience Letters.

[15]  R. Miall,et al.  Brain activation patterns during measurement of sub- and supra-second intervals , 2003, Neuropsychologia.

[16]  J. Tanji,et al.  Spatial distribution of cingulate cells projecting to the primary, supplementary, and pre-supplementary motor areas: a retrograde multiple labeling study in the macaque monkey , 2001, Neuroscience Research.

[17]  S. D. Lima,et al.  Duration discrimination of filled and empty auditory intervals: Cognitive and perceptual factors , 1991, Perception & psychophysics.

[18]  Stephen McAdams,et al.  The neuroanatomical substrate of sound duration discrimination , 2002, Neuropsychologia.

[19]  J A Obeso,et al.  The anatomical basis of somaesthetic temporal discrimination in humans. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[20]  C. Frith,et al.  Differential Activation of Right Superior Parietal Cortex and Intraparietal Sulcus by Spatial and Nonspatial Attention , 1998, NeuroImage.

[21]  M. Inase,et al.  Corticostriatal and corticosubthalamic input zones from the presupplementary motor area in the macaque monkey: comparison with the input zones from the supplementary motor area , 1999, Brain Research.

[22]  M. Jahanshahi,et al.  Time estimation and reproduction is abnormal in Parkinson's disease. , 1992, Brain : a journal of neurology.

[23]  Stephen M. Rao,et al.  The evolution of brain activation during temporal processing , 2001, Nature Neuroscience.

[24]  G. V. Van Hoesen,et al.  Frontal granular cortex input to the cingulate (M3), supplementary (M2) and primary (M1) motor cortices in the rhesus monkey , 1993, The Journal of comparative neurology.

[25]  J A Obeso,et al.  Temporal discrimination is abnormal in Parkinson's disease. , 1992, Brain : a journal of neurology.

[26]  Satoru Miyauchi,et al.  Dorsal visual cortex activity elicited by posture change in a visuo-tactile matching task , 2002, Neuroreport.

[27]  R. Harris-Warrick,et al.  Aminergic modulation of graded synaptic transmission in the lobster stomatogastric ganglion , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  P. Strick,et al.  Basal-ganglia 'projections' to the prefrontal cortex of the primate. , 2002, Cerebral cortex.

[29]  Kevin J. Riggs Thinking harder about false belief , 2005, Trends in Cognitive Sciences.

[30]  T. Rammsayer,et al.  Neuropharmacological Evidence for Different Timing Mechanisms in Humans , 1999, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[31]  M. Walton,et al.  Interactions between decision making and performance monitoring within prefrontal cortex , 2004, Nature Neuroscience.

[32]  R. Knight,et al.  Cortical Networks Underlying Mechanisms of Time Perception , 1998, The Journal of Neuroscience.

[33]  F. Vidal,et al.  Functional Anatomy of the Attentional Modulation of Time Estimation , 2004, Science.

[34]  Salvatore M Aglioti,et al.  Temporal discrimination of cross-modal and unimodal stimuli in generalized dystonia , 2003, Neurology.

[35]  C. Gallistel,et al.  Toward a neurobiology of temporal cognition: advances and challenges , 1997, Current Opinion in Neurobiology.

[36]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

[37]  M. Nicolelis,et al.  Interval timing and the encoding of signal duration by ensembles of cortical and striatal neurons. , 2003, Behavioral neuroscience.

[38]  Laura Bertolasi,et al.  Temporal processing of visuotactile and tactile stimuli in writer's cramp , 2003, Annals of neurology.

[39]  A. Friederici,et al.  Time Perception and Motor Timing: A Common Cortical and Subcortical Basis Revealed by fMRI , 2000, NeuroImage.

[40]  Jonathan D. Cohen,et al.  Anterior Cingulate Conflict Monitoring and Adjustments in Control , 2004, Science.

[41]  J. Mazziotta,et al.  Brain Activation Induced by Estimation of Duration: A PET Study , 1996, NeuroImage.