Elsevier

Brain Research

Volume 1217, 27 June 2008, Pages 171-178
Brain Research

Research Report
Functional contributions of the basal ganglia to emotional prosody: Evidence from ERPs

https://doi.org/10.1016/j.brainres.2008.04.032Get rights and content

Abstract

The basal ganglia (BG) have been functionally linked to emotional processing [Pell, M.D., Leonard, C.L., 2003. Processing emotional tone form speech in Parkinson's Disease: a role for the basal ganglia. Cogn. Affec. Behav. Neurosci. 3, 275–288; Pell, M.D., 2006. Cerebral mechanisms for understanding emotional prosody in speech. Brain Lang. 97 (2), 221–234]. However, few studies have tried to specify the precise role of the BG during emotional prosodic processing. Therefore, the current study examined deviance detection in healthy listeners and patients with left focal BG lesions during implicit emotional prosodic processing in an event-related brain potential (ERP)-experiment. In order to compare these ERP responses with explicit judgments of emotional prosody, the same participants were tested in a follow-up recognition task. As previously reported [Kotz, S.A., Paulmann, S., 2007. When emotional prosody and semantics dance cheek to cheek: ERP evidence. Brain Res. 1151, 107–118; Paulmann, S. & Kotz, S.A., 2008. An ERP investigation on the temporal dynamics of emotional prosody and emotional semantics in pseudo- and lexical sentence context. Brain Lang. 105, 59–69], deviance of prosodic expectancy elicits a right lateralized positive ERP component in healthy listeners. Here we report a similar positive ERP correlate in BG-patients and healthy controls. In contrast, BG-patients are significantly impaired in explicit recognition of emotional prosody when compared to healthy controls. The current data serve as first evidence that focal lesions in left BG do not necessarily affect implicit emotional prosodic processing but evaluative emotional prosodic processes as demonstrated in the recognition task. The results suggest that the BG may not play a mandatory role in implicit emotional prosodic processing. Rather, executive processes underlying the recognition task may be dysfunctional during emotional prosodic processing.

Introduction

Successful emotional communication is crucial to social interaction. The tone of voice, or emotional prosody, helps to understand how people feel. In particular, listeners must continually monitor and rapidly detect changes in their interlocutor's mood in order to adapt their behavior accordingly during speech perception. Imagine a telephone conversation in which your interlocutor is simultaneously reading his credit card bill, and realizes that his wife has spent $1000 on shoes in the past month. It might well be that you are confronted with an abrupt change of tone of voice—from carrying no affect (hereafter referred to as neutral) to an angry tone of voice. Many other instances in which there are dynamic, and sometimes abrupt deviations in emotional prosody occur regularly in spoken interactions.

We previously showed that participants can very quickly detect changes in emotional prosodic contours, and that such change detection is linked to a right-lateralized positive event-related brain potential (ERP; hereafter referred to as prosodic expectancy positivity, or PEP; Kotz and Paulmann, 2007). Moreover, this deviance detection does not vary as a function of valence (positive vs. negative, Kotz and Paulmann, 2007), or by emotional category (Paulmann and Kotz, 2008). We suggest that the PEP reflects rapid on-line detection of acoustic changes in vocal expressions of emotions independent of attention (implicit and explicit processing), sentence modality (lexical and non-lexical sentence stimuli), and valence (positive and negative). Other positivities elicited by linguistic prosodic deviations, such as the P800 (Astésano et al., 2004) or the closure-positive shift (CPS; Steinhauer et al., 1999) often have a later onset and longer latency than the PEP. For example, the P800 onsets 800 ms post-stimulus (Astésano et al., 2004), while the PEP is elicited approximately 300 ms after the critical position in a sentence. We have proposed that the earlier onset and shorter duration of the PEP may be correlated with the point in time that a stimulus takes on emotional significance (see Paulmann et al., 2008a, Paulmann et al., 2008b).1 Emotional significance is likely to be conveyed by acoustic parameters, such as pitch, intensity, and more fine-grained parameters, such as voice quality. One major open question is which neural substrates and which underlying mechanism(s) may contribute to this type of significance detection, in particular when prosodic expectancy is violated.

Considerable research has investigated whether emotional prosodic processing relies on hemispheric specialization. Although ample evidence suggests that the right hemisphere (RH) plays a central role in the decoding of emotional prosody (e.g., Breitenstein et al., 1998, Heilman et al., 1984, Pell, 1998), more recent results indicate that emotional prosodic processing involves a bilaterally distributed neural network (Gandour et al., 2004, Kotz et al., 2003; see also Ross et al., 1997, Kotz et al., 2006, for explanations on heterogeneous lateralization results). In fact, there is growing consensus that the RH plays relative rather than absolute dominance in emotional prosodic processing (see Pell, 2006). While the RH is implicated in the analysis of emotional prosodic attributes, the left hemisphere (LH) is often linked to linguistically-based processing (e.g., Friederici and Alter, 2004, Pell, 2006, Van Lancker Sidtis et al., 2006). Furthermore, one may argue that the LH serves an integrative function combining verbal-semantic processes with emotion- or pitch-related processes (Pell, 2006, Schirmer and Kotz, 2006).

Next to the issue of lateralization, research has explored the brain network supporting emotional prosodic processing. Evidence suggests that this network is not limited to cortical brain areas, but also involves subcortical areas such as the basal ganglia (BG) (e.g., Cancelliere and Kertesz, 1990, Pell and Leonard, 2003, Pell, 2006, Van Lancker Sidtis et al., 2006). Indeed, the importance of the BG in emotional prosody processing has gained support from patient studies (e.g., Breitenstein et al., 1998, Breitenstein et al., 2001) as well as from functional imaging studies with healthy participants (e.g., Kotz et al., 2003, Wildgruber et al., 2002). It is proposed that the BG play a role in the sequencing of auditory affective information (Pell and Leonard, 2003, Meyer et al., 2004), i.e., it is suggested that BG impairment may cause reduced capability to encode emotionality from affective prosodic cue sequences (e.g., pitch and intensity variations during an emotional utterance; see Pell and Leonard, 2003). Furthermore, it is proposed that this process should interact with cortical associative functions in order to allow evaluating prosodic emotional cues (see Schirmer and Kotz, 2006). It should be critically noted though that neither fMRI nor behavioral patient studies can specify the temporal dynamics of emotional prosodic processing. As behavioral and ERP measures may tap into different processing stages, a combination of a both temporally sensitive measure and behavior should shed more light on process-specific and task-specific effects, and should allow specifying the nature of previously described emotional deficits in BG-patients more precisely. We therefore applied both measures—ERPs and behavior in BG-patients and healthy controls while they listened to emotional prosodic sentences.

As reviewed above, some research suggests functionally (emotion vs. linguistic) dependent lateralization of prosodic information processing (Pell, 2006, Schirmer and Kotz, 2006, Pihan et al., 2000). Also, there is some evidence that left- and right-sided lesion patients differ in their use of acoustic cues. For example, right-sided lesion patients are often reported to rely more on temporal cues, while left-sided patients rely more on fundamental frequency (Robin et al., 1990, Van Lancker and Sidtis, 1992). This has led to the hypothesis that the LH is involved in processing temporal cues, while the RH is dominantly engaged in pitch processing. One major motivation of the current study is to find out whether such lateralization principles also apply to patients with subcortical lesions. The detection of abrupt prosodic deviances as described above is clearly based on evaluating pitch change (amongst other acoustical parameters). Hence, to test whether the left BG similarly to left cortical areas do not rely on pitch-related processes, we investigated emotional prosodic change detection in left-sided BG lesion patients in an on-line ERP experiment. Adopting our previously established cross-splicing paradigm (Kotz and Paulmann, 2007, Paulmann and Kotz, 2008), we aimed to replicate PEP responses in healthy participants, and in left-sided BG-patients. Secondly, we asked participants to recognize the emotional intonation of pseudo-sentences in a follow-up behavioral experiment. If emotional prosodic deviance detection is impaired in BG-patients, this should result in a reduced or missing PEP response. If, however, the online processing of emotionally laden acoustic cues is unimpaired in left BG-patients, healthy controls and BG-patients should show a comparable PEP response. The question remains whether task-related evaluation of emotional prosodic stimuli is affected in BG-patients. If this was the case, we should replicate previously reported emotional prosody recognition deficits as reflected in lower recognition rates for BG-patients than healthy controls in the behavioral follow-up experiment.

Section snippets

Results

Behavioral results for the ERP experiment were not analyzed because previous research (Kotz and Paulmann, 2007, Paulmann and Kotz, 2008) has found no effects for prosodic expectancy violations in reaction times or percentage correct responses in healthy participants.

Discussion

The present study aimed to substantiate why the left BG similarly to left temporal brain regions may not play a significant role in the detection of rapid pitch changes in emotional prosodic contours. Both healthy controls and BG-patients showed a PEP response to emotional prosodic expectancy violations. This replicates our previous results in younger healthy participants (Kotz and Paulmann, 2007, Paulmann and Kotz, 2008) but extends the results to an aging healthy population (mean age:

Participants

Twelve chronic patients (1 female, all right-handed; mean age: 49.2 years) with focal lesions in the striatum participated in the study after giving informed consent. Lesions resulted from LH insults: ischemic stroke (n = 3), embolic stroke (n = 3), hemorrhage (n = 3), intracerebral bleeding (ICB; n = 3), or arterio-arterial infarction (n = 1). The average time post-lesion was: 4.6 years (range 1.8–7.1). Lesion sites were determined by (T1- and T2-weighted) anatomical MRI datasets from a 3.0 T system

Acknowledgments

The authors wish to thank Cornelia Schmidt for her help with data acquisition, Anke Marschhauser for providing neuropsychological test scores, Burkhard Maess for his help with data filtering, and Kerstin Flake for her help with preparing graphical illustrations. This work was supported by the German Research Foundation (DFG FOR 499 to S.A. Kotz) and by the Canadian Institutes of Health Research (Operating grant to M.D. Pell & S.A. Kotz).

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