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Discussion forum

How are innate emotions evoked? Taketoshi Ono* and Hisao Nishijo System Emotional Science, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, Toyama, Japan

We read with great interest the book and its precis by Rolls (2014a,b). He defines emotions as states in organisms that are elicited by reinforcements (rewards and punishments) and motivation as a state in which organisms are working for a goal to acquire or avoid reinforcements. Based on Darwin’s theory of evolution (1859), Rolls proposes that emotions have an important evolutionary role in specifying a goal (rewards) (e.g., rewards that elicit positive emotions are necessary for the survival of organisms). According to Rolls’ theory, neural mechanisms are hierarchically implemented in cortical systems. Stimuli (objects) are consciously represented in the higher association areas, such as the inferotemporal cortex, and this information is then sent to the amygdala and orbitofrontal cortex that code emotions and the emotional values of the stimuli. Finally, the value information is transferred to other areas, including the anterior cingulate cortex and basal ganglia, in order to select optimal actions required to acquire rewards. These theories elegantly explain human conscious emotions and behaviors. Furthermore, the theories and hypotheses for human higher cognitive and conscious processes proposed in the book can be testable by computer simulation. This method could uncover the neural mechanisms of emotions in humans at the cellular and system levels. We completely agree with the Darwinian account of emotion (Ono & Nishijo, 1992), as Rolls has proposed. In addition to the cortical systems that Rolls says is important for emotion processing, we would like to stress a role of subcortical sensory systems, such as subcortical fear modules (LeDoux, 2012), in unconscious innate emotions, which might also affect behavior and decision making in primates. Rolls has suggested that early stages in sensory processing may evoke emotional responses in non-primates, such as rodents. We similarly suggest that the phylogenetically old subcortical

sensory systems for innate behaviors that detect biologically significant stimuli (e.g., snakes or faces) are also functional in primates and might be involved in unconscious emotion, as in rodents. The values of the stimuli for innate behaviors might be encoded into genes by natural selection. This is why these stimuli can evoke behavioral responses without learning. These subcortical sensory systems for innate behaviors may correspond to the survival circuits proposed by LeDoux (2012). Here, we argue a role of subcortical sensory systems in emotional processing in primates, and subcortical influences on cortical processing of emotion-laden stimuli. The recognition of snakes is innate in primates (Sewards & Sewards, 2002). A behavioral study has shown that even laboratory-reared monkeys display avoidance responses to toy snakes (Cook & Mineka, 1989). Humans and monkeys can more easily associate snakes than most other stimuli with ¨ hman & Mineka, 2001), and snakes automatically, shock (O ¨ hman, Flykt, & and in shorter latencies, capture attention (O Esteves, 2001). Furthermore, adult humans and young children detect more rapidly snakes displaying striking posture than snakes without such posture (Masataka, Hayakawa, & Kawai, 2010). The young children in this experiment were reported to have never seen any images of snakes before the experiment. These findings suggest that there might be a set of innate brain structures (fear module) that detect evolu¨ hman & tionary fear-relevant stimuli, such as snakes (O Mineka, 2003). Anthropological studies have also suggested that snakes have driven the evolution of primate 3D, color vision to quickly detect serpentine predators (snake detection theory) (Isbell, 2009). Because it has been suggested that the primate pulvinar has evolved to detect snakes (Isbell, 2009), we analyzed neuronal responses in the monkey pulvinar during a delayed

* Corresponding author. System Emotional Science, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, Sugitani 2630, Toyama 930-0194, Japan. E-mail address: [email protected] (T. Ono). http://dx.doi.org/10.1016/j.cortex.2014.03.007 0010-9452/ª 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Ono, T., & Nishijo, H., How are innate emotions evoked?, Cortex (2014), http://dx.doi.org/ 10.1016/j.cortex.2014.03.007


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non-matching-to-sample task in which monkeys were required to discriminate among 4 categories of visual stimuli [photos of snakes (snakes facing monkeys and attacking toward the sides), faces (angry and neutral monkey faces), hands, and simple geometrical patterns] (Le et al., 2013). The responses to the snakes were unique. First, the percentage of neurons that responded more strongly to the snakes was significantly greater than that of the neurons that responded more strongly to the other stimuli. Second, the response latencies to the snakes were shorter than those to the other stimuli. Third, low-pass filtering of the images did not affect the responses, but high-pass filtering decreased the responses. In addition, we have reported that superior collicular and pulvinar neurons respond faster to face-like stimuli than simple geometrical figures (Nguyen et al., 2013, 2014) and that monkeys with bilateral lesions of the superior colliculus, which projects to the pulvinar, did not avoid a snake model (Maior et al., 2011). These results indicate that the pulvinar processes fast and coarse visual information of snakes and suggest that the detection of the serpentine form is one of the major functions of the subcortical visual pathway, including the pulvinar. Recent neuropsychological studies have suggested that this subcortical visual pathway is functional in humans. A patient with blindsight and striate cortex damage has been reported to show specific activation in the superior colliculus, pulvinar, and amygdala in response to angry emotional actions in the blind hemifield (Van den Stock et al., 2011). In addition, a patient with bilateral destruction of the visual cortex has been reported to show amygdala activation in response to direct gaze (Burra et al., 2013). This colliculopulvinar pathway has been implicated as a fast route of visual information in the fear module circuitries in humans ¨ hman, & Dolan, 1999; (Csatho, Tey, & Davis, 2008; Morris, O Tamietto & de Gelder, 2010). The characteristics of the monkey pulvinar neuronal responses to snakes that were observed in our experiment (i.e., short response latencies to snakes and dependence on low spatial frequency) corroborate the view that the pulvinar plays a crucial role in this fear module. Because the pulvinar has intimate anatomical connections with the cortical system (Pessoa & Adolphs, 2010), the subcortical visual system could modulate the cortical conscious system that has been proposed by Rolls (2014a,b). Since response latencies of the superior collicular and pulvinar neurons were shorter than cortical neurons (Nguyen et al., 2013, 2014; Le et al., 2013), the subcortical pathway may provide coarse information of innate stimuli with the cortical system before information from the fine sensory systems (e.g., parvocellular visual pathway) arrives at the cortical system. It has been noted that subcortical visual pathways directly project to the autonomic and motor areas in the brainstem and bypass the cortical system. Therefore, innate stimuli (e.g., snakes) could unconsciously induce emotional expression (various autonomic and motor responses) through these subcortical pathways. However, these peripheral responses elicited by innate stimuli could later induce conscious emotions through the feedback system from the periphery to the brain, especially the orbitofrontal cortex and amygdala, as has been proposed by Damasio (1996), James (1884), and Lange

(1887). These processes could explain some of the irrational fears of innate stimuli. Thus, we would like to propose parallel emotional neural circuits in primates: one involving the coarse subcortical emotional neural circuit connecting innate stimuli and autonomic and motor outputs, and the other involving the fine and flexible neural circuits that include the cortical system proposed by Rolls. The feedback systems connect these parallel neural circuits. In conclusion, the subcortical systems may simultaneously code “what the innate stimulus is” as well as “what the value of the innate stimulus is” although its processing level is low, and could affect cortical processing of emotion-laden stimuli.

Acknowledgments This work was supported partly by the Japan Society for the Promotion of Science Asian Core Program and the Ministry of Education, Science, Sports and Culture, Grant-in-Aid for Scientific Research (B) (25290005).


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Received 20 February Reviewed 28 February Revised 6 March Accepted 11 March

2014 2014 2014 2014

Please cite this article in press as: Ono, T., & Nishijo, H., How are innate emotions evoked?, Cortex (2014), http://dx.doi.org/ 10.1016/j.cortex.2014.03.007

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