Does it talk the talk? On the role of basal ganglia in emotive speech processing

Uri Hasson¹, Daniel A. Llano², Gabriele Miceli¹, & Anthony Steven Dick³

1 Center for Mind/Brain Sciences and Department of Psychology and Cognitive Science, University of Trento, Mattarello, Italy;

2 School of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801;

3 Department of Psychology, Florida International University, Miami, FL 33199.. Trento, Italy.

Corresponding author:

Uri Hasson, PhD

Center for Mind & Brain Sciences (CIMeC)

University of Trento, Mattarello (TN), Italy, 38123

Email: uri.hasson@unitn.it

Phone: +39-3203055679

Abstract

Ackermann et al.’s phylogenetic account of speech argues that the basal ganglia imbue speech with emotive content. However, a body of work on auditory/emotive processing is inconsistent with attributing this function exclusively to these structures. The account further overlooks the possibility that the emotion-integration function may be at least in part mediated by the cortico-ponto-cerebellar system.

Introduction

Ackermann et al.’s phylogenetic account of speech development hinges, in part, on premises related to the role of basal ganglia (BG) in adult human speech production. It argues that in adults, BG imbue speech with emotive content. While the model targets an important and neglected issue, we argue that it suffers from two structural weaknesses: First, it does not sufficiently consider studies of the role of BG in auditory and emotive processing such as those showing that BG damage does not disrupt emotive processing in speech. Second, the argument also overlooks the possibility that the role attributed to the BG may be at least in part mediated by a different system – the cortico-ponto-cerebellar system. We believe the authors’ account would be much strengthened if they address these points, which we detail in turn.

Viability of BG as a speech/emotion synthesizer.

A principle incorporated in contemporary models of speech production is that production occurs under one or more levels of feedback, where potential production errors are monitored either after utterance production (sensory feedback) or prior to it (via internal models; e.g., Hickok 2012). Ackermann et al. do not couch their account in an existing speech-production model and leave the issue of feedback underspecified. Nonetheless, if the BG were responsible for imbuing speech with emotive content, it would be expected to have the capacity to monitor and correct for related errors, that is, evaluate that the intended emotive tone/prosody was instantiated. However, BG are a weak candidate for such a function. The authors ignore studies indicating (1) that the auditory response in BG is temporally insufficient to provide feedback (Langers & Melcher 2011) and that it has limited functional connectivity with areas of the temporal cortex mediating language processing (Choi et al. 2012), (2) that emotive speech processing is mediated mainly by lateral temporal systems while excluding the BG (Kotz et al. 2013; Wildgruber et al. 2006), and most importantly (3) that individuals with BG infarcts are equally sensitive to emotional speech variations as control populations (Paulmann et al. 2008; 2011). These three points argue against the authors’ claim that adding prosody to speech depends on integrity of striatum.

The suggested account relies on two additional premises that are not strongly supported by the literature. The first: That in adults, the BG can afford coding for emotion since adult perisylvian regions code for syllable motor programs, independently of the BG. Empirical support for this point is tenuous at best; studies using manipulations of syllable frequency have either reported null results (Brendel et al. 2011; Riecker et al. 2008) or documented effects in the anterior insula (Carreiras et al. 2006). The second: The BG can merge emotional content due to cross talk between cortico-striatal-thalamic circuits. Although there is anatomical evidence for cross talk across BG circuits in animal models (Haber 2003), the functional significance of these needs to be fleshed out.

On the consideration of alternatives

A BG-oriented account should address questions such as those above, and equally importantly argue why the BG is the strongest neurobiological candidate for mediating the function in question. The authors do not make such an argument, which is unfortunate since much of the neurobiological argument made here for BG could be made effectively for other structures, such as the cerebellum.

The involvement of the cerebellum in emotional processing is well established. It is implicated in self-generation of various emotional states (Damasio et al. 2000), with different emotions evoking distinct activity patterns in the structure (Baumann & Mattingley 2012). Damage to the cerebellum affects emotional processing. In animal models, early cerebellar lesions can lead to disrupted emotional processing (Bobee et al. 2000), and in human adults, the cerebellar cognitive affective syndrome (CCAS; Schmahmann & Sherman 1998) is a recognized clinical entity associated with blunting of affect. CCAS has been attributed to damage to the posterior vermis, which reduces the cerebellar contribution to perisylvian cortical areas via its outflow to the ventral tier thalamic nuclei (Stoodley & Schmahmann 2010).

Arguments used by Ackermann et al. in support of their BG hypothesis could also be applied to the cerebellum. For example, FOXP2 expression is found in the cerebellum as well as the caudate (Lai et al. 2003; Watkins et al. 2002), and as shown by Ackermann et al. (1992), cerebellar lesions are associated with dysarthia. In addition, activity in the cerebellum, but not BG, discriminates emotive aspects of speech (Kotz et al. 2013). Furthermore, the cerebellum has the capacity for generating an internal forward model of motor-to-auditory predictions of the sort needed to evaluate whether the intended emotive aspect has been communicated (Knolle et al. 2013). While there is no direct examination of this issue for BG, work on motor control suggests that functionally, BG may implement open- rather than closed-loop control of motor actions (Gabrieli et al. 1997).

It is important to point out that these explanations are not mutually exclusive. Cerebellar and BG circuits involved with language converge at the ventral anterior nucleus of the thalamus, which has also been implicated in language, and can serve as a nidus for cortical feedback via cortico-thalamic projections (Crosson 2013). Further, cerebellar outflow can directly influence the BG and vice versa (Bostan et al. 2013), suggesting that attributing the emotional content of speech to either of these two systems in isolation may not be possible. Given this connectivity, it may be that the cerebellum drives emotion-carrying vocalizations by involving BG, or that the BG trigger emotional behavior that is ultimately modulated by the cerebellum, as would be consistent with a CCAS syndrome. However, data on this issue are lacking.

Summary

Arguing that the BG can imbue speech with emotional content is a significant claim and, as such, requires additional evidence, accompanied by careful consideration of alternative accounts. We hope this commentary will result in more detailed examination of the aforementioned issues.

References

Ackermann, H., Vogel, M., Petersen, D. & Poremba, M. (1992) Speech deficits in ischaemic cerebellar lesions. Journal of Neuroscience 239(4):223–27. [UH]

Baumann, O. & Mattingley, J. B. (2012) Functional topography of primary emotion processing in the human cerebellum. NeuroImage 61(4):805–11. doi: 10.1016/j.neuroimage.2012.03.044 [UH]

Bobee, S., Mariette, E., Tremblay-Leveau, H. & Caston, J. (2000) Effects of early midline cerebellar lesion on cognitive and emotional functions in the rat. Behavioural Brain Research 112(1–2):107–17. [UH]

Bostan, A. C., Dum, R. P. & Strick, P. L. (2013) Cerebellar networks with the cerebral cortex and basal ganglia. Trends in Cognitive Sciences 17(5):241–54. doi: 10.1016/j.tics.2013.03.003 [UH]

Brendel, B., Erb, M., Riecker, A., Grodd, W., Ackermann, H. & Ziegler, W. (2011) Do we have a “mental syllabary” in the brain? An fMRI study. Motor Control 15(1):34–51. [UH]

Carreiras, M., Mechelli, A. & Price, C. J. (2006) Effect of word and syllable frequency on activation during lexical decision and reading aloud. Human Brain Mapping 27(12):963–72. doi: 10.1002/hbm.20236 [UH]

Choi, E. Y., Yeo, B. T. & Buckner, R. L. (2012) The organization of the human striatum estimated by intrinsic functional connectivity. Journal of Neurophysiology 108(8):2242–63. doi: 10.1152/jn.00270.2012 [UH]

Crosson, B. (2013) Thalamic mechanisms in language: A reconsideration based on recent findings and concepts. Brain and Language 126(1):73–88. doi: 10.1016/j.bandl.2012.06.011 [UH]

Damasio, A. R., Grabowski, T. J., Bechara, A., Damasio, H., Ponto, L. L., Parvizi, J. & Hichwa, R. D. (2000) Subcortical and cortical brain activity during the feeling of self-generated emotions. Nature Neuroscience 3(10):1049–56. doi: 10.1038/79871 [UH]

Gabrieli, J. D., Stebbins, G. T., Singh, J., Willingham, D. B. & Goetz, C. G. (1997) Intact mirror-tracing and impaired rotary-pursuit skill learning in patients with Huntington’s disease: Evidence for dissociable memory systems in skill learning. Neuropsychology 11(2):272–81. [UH]

Haber, S. N. (2003) The primate basal ganglia: Parallel and integrative networks. Journal of Chemical Neuroanatomy 26(4):317–30. [UH]

Hickok, G. (2012) Computational neuroanatomy of speech production. Nature Reviews. Neuroscience 13(2):135–45. doi: 10.1038/nrn3158 [UH]

Knolle, F., Schroger, E. & Kotz, S. A. (2013) Cerebellar contribution to the prediction of self-initiated sounds. Cortex 49(9):2449–61. doi: 10.1016/j.cortex.2012.12.012 [UH]

Kotz, S. A., Kalberlah, C., Bahlmann, J., Friederici, A. D. & Haynes, J. D. (2013) Predicting vocal emotion expressions from the human brain. Human Brain Mapping 34(8):1971–81. doi: 10.1002/hbm.22041 [UH]

Lai, C. S., Gerrelli, D., Monaco, A. P., Fisher, S. E. & Copp, A. J. (2003) FOXP2 expression during brain development coincides with adult sites of pathology in a severe speech and language disorder. Brain 126(Pt 11):2455–62. doi: 10.1093/brain/awg247 [UH]

Langers, D. R. & Melcher, J. R. (2011) Hearing without listening: Functional connectivity reveals the engagement of multiple nonauditory networks during basic sound processing. Brain Connect 1(3):233–44. doi: 10.1089/brain.2011.0023 [UH]

Paulmann, S., Ott, D. V. & Kotz, S. A. (2011) Emotional speech perception unfolding in time: The role of the basal ganglia. PLOS ONE 6(3):e17694. doi: 10.1371/journal.pone.0017694 [UH]

Paulmann, S., Pell, M. D. & Kotz, S. A. (2008) Functional contributions of the basal ganglia to emotional prosody: Evidence from ERPs. Brain Research 1217:171–78. doi: 10.1016/j.brainres.2008.04.032 [UH]

Riecker, A., Brendel, B., Ziegler, W., Erb, M. & Ackermann, H. (2008) The influence of syllable onset complexity and syllable frequency on speech motor control. Brain and Language 107(2):102–13. doi: 10.1016/j.bandl.2008.01.008 [UH]

Schmahmann, J. D. & Sherman, J. C. (1998) The cerebellar cognitive affective syndrome. Brain 121 ( Pt 4):561–79. [UH]

Stoodley, C. J. & Schmahmann, J. D. (2010) Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex 46(7):831–44. doi: 10.1016/j.cortex.2009.11.008 [UH]

Watkins, K. E., Vargha-Khadem, F., Ashburner, J., Passingham, R. E., Connelly, A., Friston, K. J., Frackowiak, R. S., Mishkin, M., Gadian, D. G. (2002) MRI analysis of an inherited speech and language disorder: Structural brain abnormalities. Brain 125(Pt 3):465–78. [UH]

Wildgruber, D., Ackermann, H., Kreifelts, B. & Ethofer, T. (2006) Cerebral processing of linguistic and emotional prosody: fMRI studies. Progress in Brain Research 156:249–68. doi: 10.1016/S0079-6123(06)56013-3 [UH]