Impaired Feedforward Control and Enhanced Feedback Control of Speech in Patients with Cerebellar Degeneration

Abstract

The cerebellum has been hypothesized to form a crucial part of the speech motor control network. Evidence for this comes from patients with cerebellar damage, who exhibit a variety of speech deficits, as well as imaging studies showing cerebellar activation during speech production in healthy individuals. To date, the precise role of the cerebellum in speech motor control remains unclear, as it has been implicated in both anticipatory (feedforward) and reactive (feedback) control. Here, we assess both anticipatory and reactive aspects of speech motor control, comparing the performance of patients with cerebellar degeneration and matched controls. Experiment 1 tested feedforward control by examining speech adaptation across trials in response to a consistent perturbation of auditory feedback. Experiment 2 tested feedback control, examining online corrections in response to inconsistent perturbations of auditory feedback. Both male and female patients and controls were tested. The patients were impaired in adapting their feedforward control system relative to controls, exhibiting an attenuated anticipatory response to the perturbation. In contrast, the patients produced even larger compensatory responses than controls, suggesting an increased reliance on sensory feedback to guide speech articulation in this population. Together, these results suggest that the cerebellum is crucial for maintaining accurate feedforward control of speech, but relatively uninvolved in feedback control.SIGNIFICANCE STATEMENT Speech motor control is a complex activity that is thought to rely on both predictive, feedforward control as well as reactive, feedback control. While the cerebellum has been shown to be part of the speech motor control network, its functional contribution to feedback and feedforward control remains controversial. Here, we use real-time auditory perturbations of speech to show that patients with cerebellar degeneration are impaired in adapting feedforward control of speech but retain the ability to make online feedback corrections; indeed, the patients show an increased sensitivity to feedback. These results indicate that the cerebellum forms a crucial part of the feedforward control system for speech but is not essential for online, feedback control.

Keywords: ataxic dysarthria; cerebellum; feedback control; feedforward control; speech; speech motor control.

Copyright © 2017 the authors 0270-6474/17/379249-10$15.00/0.

Figures

Figure 1.

Schematic of auditory feedback manipulation process. The participant's speech is recorded via a head-mounted microphone and passed to the computer. The digital signal processing software estimates the vowel formants (F1–F3, red lines), introduces a desired shift (shown in blue as a negative displacement of F1), and resynthesizes the speech for playback to the participant via over-the-ear headphones. This process induces a change in the perceived vowel. In this example, the production of “head” would sound like “hid.”

Figure 2.

Experimental design and results from Experiment 1 on feedforward adaptation. a, Schedule of perturbations in Experiment 1. Conditions of interest are the gradual and abrupt perturbations. b, d, Behavioral results from noncatch trials for gradual and abrupt perturbations, respectively. Productions are grouped into bins of 10. Error bars indicate SE. Light gray represents probes (baseline, early, late, washout). The perturbation schedule is shown below the behavioral results (black). There was no difference in results between the two conditions. f, Control (red) and patient (blue) productions in the early probe, late probe, and washout phases, normalized to the baseline values. *Significant difference from baseline. c, e, Productions during the catch trials in the gradual and abrupt conditions, respectively. In these trials, loud speech-shaped noise was used to mask feedback from the participants' speech. On these trials, participants responded by dramatically increasing F1. This type of increase is typical in loud noise and makes it problematic to measure an adaptive response. Nonetheless, the trend in both cases is that CD patients produce a reduced increase in F1 compared with healthy controls.

Figure 3.

Results from Experiment 2 on feedback compensation. a, Response of healthy controls (red) and CD patients (blue) to unexpected upward (150 Hz, solid) and downward (−150 Hz, dotted) perturbations of F1. The functions represent differences on perturbation trials, relative to baseline, shown over time averaged across participants. Shading represents SE. b, Maximum response (average from 300 to 400 ms after vowel onset) for the unperturbed, shift-up, and shift-down conditions. Means are shown along with individual responses (black circles). c, Example of the spline-fitting method used to calculate response latencies. d, Mean latencies and individual responses. There were no differences between groups or perturbation directions. *Significant difference from baseline.