Elsevier

Cortex

Volume 71, October 2015, Pages 332-340
Cortex

Note
Striatal contributions to sensory timing: Voxel-based lesion mapping of electrophysiological markers

https://doi.org/10.1016/j.cortex.2015.07.016Get rights and content

Abstract

To achieve precise timing, the brain needs to establish a representation of the temporal structure of sensory input and use this information to generate timely responses. These operations engage the basal ganglia. Current research in this direction is limited by reliance on animal models, motor and/or offline tasks, small sample sizes, the low temporal resolution of functional magnetic resonance imaging, and the study of progressive neurodegeneration. Here, we combine the excellent temporal resolution of electrophysiological potentials with the high spatial resolution of structural neuroimaging to investigate basal ganglia contributions to sensory timing. Chronic-stage lesion patients and healthy controls listened to pure-tone sequences differing exclusively in temporal regularity. Event-related potentials (ERPs) indicate a selective indifference against this manipulation in patients, attributable to the striatal part of the basal ganglia on the basis of a lesion-mapping approach. These findings provide evidence for a crucial contribution of the basal ganglia to basic sensory functioning.

Introduction

Adequate timing, defined as the ability to be in the right place at the right time, requires reactions to events in the environment and predictive adaptation of behavior in constant anticipation of the future (Bar, 2007, Schwartze and Kotz, 2013). The complex dynamics of some distinctive facets of human behavior provide ample evidence for the smooth interplay of these mechanisms. In speech and music, dance and sports, timing partly determines the quality of a message or a melody of interaction and competition.

The link between timing and efficient behavior is not always as evident as in the win-or-lose situations found in sports. Nevertheless, its existence provides a means to influence and optimize behavior via manipulations of temporal structure, i.e., the duration, temporal relation, or temporal predictability of events. Optimized behavior at one end of a spectrum, however, suggests suboptimal behavior with inadequate timing towards the other, potentially compromising the ability for predictive adaptation of behavior. Notable timing dysfunctions have been observed in neuropathologic and psychiatric conditions with relatively high prevalence, including autism, attention deficit hyperactivity disorder, schizophrenia, Huntington's and Parkinson's disease (Allman and Meck, 2012, Cope et al., 2014, Hart et al., 2012, Jones and Jahanshahi, 2014). In light of such findings, it stands to reason to what extent timing factors into seemingly non-related motor and non-motor neurocognitive functions and symptoms, if it is cause or consequence of such symptoms, and if manipulation of temporal structure may foster compensation.

Converging evidence supports the idea that classical motor areas form part of a dedicated sensorimotor system compatible with the distinction of motor and non-motor structures within particular areas (Akkal et al., 2007, Ivry and Schlerf, 2008, Strick et al., 2009). More specifically, a core network, comprising prefrontal areas and supplementary motor area but also cerebellum and basal ganglia engages in temporal processing (Coull et al., 2011, Merchant et al., 2013, Wiener et al., 2010). Accordingly, neurodegenerative diseases affecting the basal ganglia can impair motor function, but also sensory timing (Cope et al., 2014, Grahn and Brett, 2009, O'Boyle et al., 1996). Neurodegeneration in these cases is, however, progressive and not restricted to a focal area, while the typical experimental tasks involve motor components, which inevitably entail exteroceptive or proprioceptive feedback, i.e., a sensory aspect. To address these potential confounds it is necessary to define the role of specific areas of the overarching network in purely sensory timing.

Here, we use the auditory P50, an event-related potential (ERP) of the electroencephalogram (EEG) peaking at about 45–75 ms post-stimulus onset (Korzyukov et al., 2007), as a time-sensitive marker of differences in sensory timing. The P50 amplitude displays an inverse relation with predictability of stimulus type and timing, i.e., high degrees of stimulus predictability are associated with smaller relative to larger amplitudes associated with low predictability (Schwartze, Farrugia, & Kotz, 2013). Pure-tone sequences were varied along these dimensions as participants counted infrequent high-pitch deviants presented among frequent low-pitch standards (type), with either regular or irregular inter-stimulus-intervals (timing). This task established an attentive listening context, which did not require any overt behavior. In this context, the P50 served as an index for an individual's capacity to extract regular temporal relations and temporal predictability from the dynamic stimulation. Basal ganglia pathology was expected to impact on this capacity, thus diminishing the contrast between the responses obtained with regular and irregular timing. P50 amplitudes were used to perform a formal voxel-based lesion-symptom mapping (VLSM) based on volume information derived from structural MR scans of each patient to obtain more detailed information about the contribution of different basal ganglia subregions to the observed continuous neurocognitive behavior (Bates et al., 2003, Rorden et al., 2007).

Section snippets

Participants

30 right-handed chronic-stage (Mean: 8.8, SD: 3.9 years since incident) basal ganglia lesion patients (10 women) ranging in age from 31 to 78 years (Mean: 55.2, SD: 12.0) and a corresponding number of healthy controls were recruited via databases at the Max Planck Institute for Human Cognitive and Brain Sciences, Germany (Fig. 1, Table 1). Controls matched patients in terms of gender, age (±1 year, Mean: 55.4, SD: 12.2), handedness, and education (Mean: 10.1, SD: 1.1 years). Participants

Counting task

Results for the counting task in controls for regular (Mean response: 87.6, SD: 3.6; Mean percentage accuracy: 97.3%, SD: 4.0) and irregular (Mean: 93.5, SD: 4.5; Accuracy: 97.2%, SD: 4.4) stimulus presentation, as well as in patients for regular (Mean: 85.4, SD: 9.7; Accuracy: 94.4%, SD: 10.5) and irregular (Mean: 92.0, SD: 7.2; Accuracy: 93.4%, SD: 5.5) presentation suggest that participants paid attention to the sequences. The ANOVA on the actual figures yielded a significant effect of

Discussion

The current study explored the role of the basal ganglia in sensory timing on the basis of scalp-recorded electrophysiological markers (P50) and structural MR imaging in basal ganglia patients and healthy controls. In both groups, the P50 was recorded in response to auditory “oddball” sequences presented with either regular or irregular temporal structure (Schwartze et al., 2013). ERP responses in controls dissociated between frequent standard and infrequent deviant stimulus types (formal

Acknowledgments

The authors would like to thank Anne-Kathrin Franz, Heike Boethel and Ingmar Brilmayer for their support in data acquisition and pre-processing. Part of this work has been conducted while the first author was a member of staff at the Max Planck Institute for Human Cognitive and Brain Sciences in Leipzig, Germany. Support for this work came from the Max Planck Society for the Advancement of Science and DFG KO 2268/6-1 granted to S.A.K.

References (40)

  • J.V. Patterson et al.

    P50 sensory gating ratios in schizophrenics and controls: a review and data analysis

    Psychiatry Research

    (2008)
  • C.E. Schroeder et al.

    Dynamics of active sensing and perceptual selection

    Current Opinion in Neurobiology

    (2010)
  • M. Schwartze et al.

    Dissociation of formal and temporal predictability in early auditory evoked potentials

    Neuropsychologia

    (2013)
  • M. Schwartze et al.

    A dual-pathway neural architecture for specific temporal prediction

    Neuroscience and Biobehavioral Reviews

    (2013)
  • M. Schwartze et al.

    Functional dissociation of pre-SMA and SMA-proper in temporal processing

    NeuroImage

    (2012)
  • M. Wiener et al.

    The image of time: a voxel-wise meta-analysis

    NeuroImage

    (2010)
  • D. Akkal et al.

    Supplementary motor area and presupplementary motor area: targets of basal ganglia and cerebellar output

    Journal of Neuroscience

    (2007)
  • G.E. Alexander et al.

    Parallel organization of functionally segregated circuits linking basal ganglia and cortex

    Annual Review of Neuroscience

    (1986)
  • M.J. Allman et al.

    Pathophysiological distortions in time perception and timed performance

    Brain

    (2012)
  • M.J. Allman et al.

    Properties of the internal clock: first- and second-order principles of subjective time

    Annual Review of Psychology

    (2014)
  • Cited by (0)

    View full text