Motivation and Motor Control: Hemispheric Specialization for Motivation Reverses with Handedness

Motivation and Motor Control: Hemispheric Specialization for Motivation Reverses with Handedness Geoffrey Brookshire 1,2 (broog731@newschool.edu) Daniel Casasanto 1,2,3 (casasand@newschool.edu) Department of Psychology, The New School for Social Research, New York, USA Neurobiology of Language Department, Max Planck Institute for Psycholinguistics, Nijmegen, NL Donders Center for Brain, Cognition, and Behaviour, Nijmegen, NL Abstract What is the relationship between action and emotion? People tend to perform approach actions with their dominant hand and avoidance actions with their nondominant hand. In right- handers, the left frontal lobe (which controls the dominant hand) is specialized for approach-motivational states, and the right frontal lobe (which controls the nondominant hand) for avoidance-motivational states. Are brain areas that support affective motivation functionally related to areas that support approach- and avoidance-related motor actions? If so, hemispheric specialization for motivation should covary with hemispheric specialization for motor control. Here we tested this prediction, using electroencephalography (EEG) to compare resting alpha-band power in right- and left-handers. Hemispheric asymmetries in alpha-power, which indexes neural activation, were related to Behavioral Activation System (BAS) scores, which index approach-motivational tendencies. Results show that the pattern observed in right- handers reverses in left-handers, whose right hemisphere is specialized for both approach motivation and for control of dominant-hand actions. This anatomical covariation suggests a functional link between affective motivation and motor control, and also provides information crucial for developing neural therapies for affective disorders. Keywords: body-specificity hypothesis; EEG; emotion; handedness; hemispheric specialization; motivation. Introduction Emotional states are intimately linked to actions, and to the hands people use to perform them. In centuries past, sword fighters wielded the sword in the dominant hand to approach an enemy, and raised the shield with the nondominant hand to avoid attack (Pye-Smith, 1871; in Hardyck & Petrinovich, 1977). The tendency to approach with the dominant hand and avoid with the nondominant hand is evident in more ordinary motor actions, as well. When picking a piece of fruit from a tree, for example, people typically pull the fruit toward themselves (an approach action) using their dominant hand and push away the branch (an avoidance action) with the nondominant hand. When startled, people reflexively raise their nondominant hand to protect their face (Coren, 1992), leaving the dominant hand free for more complex actions. In right-handers, approach- and avoidance-related motivational states are differently lateralized in the frontal lobes of the brain. The left hemisphere subserves approach emotions and the right hemisphere, avoidance emotions (Berkman & Lieberman, 2010; Harmon-Jones, Gable, & Peterson, 2010). This means that, for right-handers, approach motivation is co-lateralized with the neural circuits primarily responsible for control of the dominant hand, and avoidance motivation with the circuits responsible for control of the nondominant hand. This may be no mere coincidence. Approach motivation may be co-lateralized with dominant-hand motor control because the dominant hand is used for approach actions. Likewise, avoidance motivation may be co-lateralized with nondominant-hand motor control because the nondominant hand is used for avoidance actions (Casasanto, 2009). Here we investigated this proposed functional connection between the neural substrates of affective motivation and motor control. If the laterality of affective motivation in right-handers results from a functional relationship between motivational states and manual motor control, then the hemispheric correlates of motivation should reverse in left-handers, for whom dominant- and nondominant-hand motor control is reversed. Alternatively, if the neural organization of motivation is functionally independent of manual motor control, a different relationship between motivation and handedness should be found. On one possibility, hemispheric specialization for motivation could be similar across most right- and left-handers, as is the case for hemispheric specialization of language (Knecht et al. 2000). Alternatively, although affective motivation appears clearly lateralized in right-handers, it could be bilaterally distributed in left-handers, as is the case for some aspects of spatial cognition (Hellige et al., 1994; Kosslyn, et al., 1989). Laterality of emotion, then and now In addition to dozens of studies confirming the hemispheric laterality of affective processing in right-handers (for review see Harmon-Jones, Gable, & Peterson, 2010), a few studies have investigated emotion processing in left-handers (Everhart, Harrison, & Crews, 1996; McFarland & Kennison, 1989; Natale, Gur & Gur, 1983; Reuter-Lorenz, Givis, & Moscovitch, 1983). Although results of these studies are consistent with the hemispheric reversal that we predict, two subsequent discoveries call their interpretation into question. These studies have two characteristics in common: they all used stimuli that varied in their emotional valence, and they all relied on lateralized presentation of stimuli to the right/left ear or the right/left visual hemifield (VHF). Over the course of three decades, the fronto-temporal hemispheric