Did I Do That? Abnormal Predictive Processes in Schizophrenia When Button Pressing to Deliver a Tone

Abstract

Motor actions are preceded by an efference copy of the motor command, resulting in a corollary discharge of the expected sensation in sensory cortex. These mechanisms allow animals to predict sensations, suppress responses to self-generated sensations, and thereby process sensations efficiently and economically. During talking, patients with schizophrenia show less evidence of pretalking activity and less suppression of the speech sound, consistent with dysfunction of efference copy and corollary discharge, respectively. We asked if patterns seen in talking would generalize to pressing a button to hear a tone, a paradigm translatable to less vocal animals. In 26 patients [23 schizophrenia, 3 schizoaffective (SZ)] and 22 healthy controls (HC), suppression of the N1 component of the auditory event-related potential was estimated by comparing N1 to tones delivered by button presses and N1 to those tones played back. The lateralized readiness potential (LRP) associated with the motor plan preceding presses to deliver tones was estimated by comparing right and left hemispheres' neural activity. The relationship between N1 suppression and LRP amplitude was assessed. LRP preceding button presses to deliver tones was larger in HC than SZ, as was N1 suppression. LRP amplitude and N1 suppression were correlated in both groups, suggesting stronger efference copies are associated with stronger corollary discharges. SZ have reduced N1 suppression, reflecting corollary discharge action, and smaller LRPs preceding button presses to deliver tones, reflecting the efference copy of the motor plan. Effects seen during vocalization largely extend to other motor acts more translatable to lab animals.

Functioning of Circuits Connecting Thalamus and Cortex

“…Also, as suggested by Figure 10, disruption of transthalamic pathways would likely lead to efference copy deficiencies. Indeed, this is precisely what is seen with schizophrenic patients: they have a variety of symptoms related to defective efference copy (44,45,126,133,158). Generally speaking, we suggest that this new concept involving transthalamic cortical pathways will prove critical in further understanding of cortical functioning in many areas of cognition, learning, memory, and attention, and also may prove a useful hypothetical framework against which to consider thalamic deficits in various clinical conditions such as schizophrenia.…”

Action-related auditory ERP attenuation: Paradigms and hypotheses

“…It is mainly supported by studies showing that in comparison to healthy controls, the magnitude of N1 attenuation is reduced in patients with schizophrenia (e.g. Ford et al, 2007, andFord et al, 2014; for a recent review see Ford & Mathalon, 2012), whose forward modeling capabilities may be impaired (Frith, Blakemore, & Wolpert, 2000). It has been also found that participants with larger readiness potential lateralization (toward the action-contra-lateral side), exhibited stronger N1-attenuation (Ford et al, 2014), which is compatible with a notion that more pronounced action-initiation activities give rise to a stronger cancellation of the auditory reafference.…”

“…Some studies find similar differences in auditory attenuation patterns between normal participants and patients with schizophrenia for speech-production and button-press actions (i.e. that the magnitude of attenuation is reduced for the patients, Ford et al, 2007, andFord et al, 2014), but direct evidence for this is yet unavailable. Since speech is probably be the best example for a behavior producing consistent patterns of auditory self-stimulation, it seems plausible that cancellation of sensory re-afference would play a role during speech production, and speech-related N1-attenuation effects reported in the literature may well reflect a corollary discharge function.…”

“…Although this may be true, currently, there is not much direct evidence for, or against this assumption. The most relevant result (Ford, Palzes, Roach, & Mathalon, 2014) is that the readiness potential preceding the action was more lateralized (De Jong, Wierda, Mulder, & Mulder, 1988;Gratton, Coles, Sirevaag, Eriksen, & Donchin, 1988; for a summary, see Eimer, 1998) when the button-pressing resulted in a tone than when it did not.…”

“…The attenuation of the P2 was also inspected in some recent studies, with many reporting significant attenuation (Knolle, Schröger, Baess, & Kotz, 2012;Horváth & Burgyán, 2013;Knolle, Schröger, & Kotz, 2013;Van Elk, Salomon, Kannape, & Blanke, 2014;Horváth 2014c), and some reporting no attenuation (Sowman, Kuusik, & Johnson, 2012;and Ford et al, 2014). N1, P2, and the T-complex are not the earliest waveforms that are attenuated in a contingent paradigm.…”