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*Correspondence: Katalin M. Gothard, department of Physiology, The college of Arizona, 1501 N. Campbell Ave. Rm., 4103, Tucson, AZ 85724 USA e-mail: ude.anozira.liame
This write-up was submitted to Decision Neuroscience, a section of the newspaper Frontiers in Neuroscience.

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Facial expression reflect decisions around the perceived an interpretation of society stimuli and also the expected socio-emotional result of responding (or not) v a reciprocating expression. The decision to produce a facial expression increase from the joint activity of a network of frameworks that encompass the amygdala and also multiple, interconnected cortical and subcortical motor areas. Reciprocal transformations in between these sensory and also motor signals offer rise to distinct brain states that promote, or impede the production of facial expressions. The muscles of the upper and also lower challenge are managed by anatomically distinctive motor areas. Facial expressions interact to a different extent the lower and upper face and also thus require distinctive patterns the neural task distributed across multiple facial motor locations in ventrolateral frontal cortex, the supplementary engine area, and two locations in the midcingulate cortex. The spread nature the the decision manifests in the share activation of multiple motor locations that start the manufacturing of facial expression. Concomitantly many areas, including the amygdala, monitor continuous overt behaviors (the expression itself) and the covert, autonomic responses the accompany emotional expressions. Together the production of face expressions is lugged into the structure of officially decision making, one important difficulty will be to incorporate autonomic and visceral states right into decisions the govern the receiving-emitting cycle of society signals.


Keywords: Macaca mulatta, society behavior, neurophysiology, cingulate cortex, emotion, neuroanatomy, face nucleus, interoception

Both human and also non-human primates use facial expressions to connect their emotions and intentions. As a motor act, a facial expression is the reflection of a decision. In a strictly society context, face expressions are produced either to initiate a social exchange, or to respond to others. The decision to create one face expression in lieu of another (or none in ~ all) counts on the emotional state the the agent, the sensory-motor state that the agent"s face, and also the evaluation of the continuous social case (e.g., what expression had been emitted, that emitted it, the agent"s partnership with the emitter, that else was present, and also what the expected social gains and also losses associated with possible responses are).

Traditionally, the circuit the controls facial expressions is conceptualized together a sequence of changes that starts with perceiving the expression of others, proceeds to extracting the socio-emotional meaning of the regarded signals, and also is completed by choosing and executing a motor response. This conceptualization suffers from number of shortcomings. It suggests unidirectionality, ignoring the duty of feedback and also the opportunity that the standing of the face and also of the autonomic nervous device can directly influence the decision. It additionally implies the the decision have the right to be confined come a framework located in between the perceptual and the engine segments of this sequence. Latent in this concept is the presumption that there should exist a neural signature of the decision at one main point within the circuit.

Alternatively, interaction with face expressions may happen as a solitary or multiple closed processing loops that bring out parallel reciprocal transformations in between sensory and motor processes. These procedures are notified by visceral inputs, and also the suspect socio-emotional value of the available choices. This alternative suggests the the decision to develop an expression does no take place at one anatomically distinctive decision node; rather it increase from the task of the entire circuit.

Recent experimental findings support this alternative. Neurons in both the primate amygdala and also midcingulate cortex respond during the tardy and production of facial expression (Livneh et al., 2012), arguing that the neural signature that the decision process could be captured by security neutral activity in this (or other) motor or limbic areas. Obtaining these data is limited only by our ability to record simultaneously the task of ensembles of neurons native multiple mind areas. Together this technology is emerging, it is precious contemplating whereby we should location the record probes to best understand the circuits that support the receiving-emitting bicycle of facial expressions? The sensory-perceptual elements of society decision making have actually received ample fist in the literature, if the motor elements have been less frequently addressed. The remainder that this write-up will to mark the anatomical facets of the motor circuit affiliated in the manufacturing of facial expression that designate these areas as potential targets because that future neurophysiological scrutiny.

Theoretically, a network connected in decisions around the use of face expressions is be intended to contain: (1) last order engine neurons that directly innervate the facial muscles, (2) a network of engine cortical neurons that innervate the last-order motor neurons, (3) neurons that signal the emotional state the the agent, (4) somatosensory-proprioceptive neurons that signal the present state that the agent"s face, and also (5) neurons that signal the motivation, or social “justification,” to do a face expression. With the exception of the engine neurons located in the facial nucleus (Jenny and Saper, 1987; Welt and Abbs, 1990) the other four varieties of neurons are situated in many areas. Because that example, sensory-motor representations of the face are discovered in the parietal cortex (Avillac et al., 2005), the insula (Schneider et al., 1993), and also in motor and premotor cortical locations (Gentilucci et al., 1988; Graziano et al., 1994). Information about the faces of rather is additionally distributed; face identity and emotional expressions space processed at the same time in the amygdala (Nakamura et al., 1992; Gothard et al., 2007), the insula (Phillips et al., 1997), and in multiple challenge patches that the temporal and frontal cortex (Hasselmo et al., 1989; Tsao et al., 2006, 2008; Romanski, 2012).


The motor control of facial expressions

Facial movements can be (1) voluntary, combination by cortical pathways, (2) reflexive, or (3) driven by main pattern generators combination by subcortical engine pathways, located greatly in the brainstem. Species-specific defensive behaviors and also vocalizations, are generally orchestrated by specialized cell clusters in the periaqueductal gray (Jürgens and Ploog, 1970; Bandler and also Shipley, 1994). Likewise the hypothalamus coordinates activity patterns that are component of more complex ritualized behaviors such as courtship and also mating, the may incorporate facial display screens (MacLean, 1990). These subcortical locations are hardly sufficient, however, come voluntarily straight a face expression towards an separation, personal, instance of interest, together it happens throughout non-ritualized society interactions. Subcortical areas might be fast and efficient come extract general information, together as peril signals (Pessoa and also Adolphs, 2010), but do not have actually the neural machine to extract from faces subtle signal that notify our moment-to-moment decisions throughout social interactions (e.g., mock or heartfelt expressions of are afraid or happiness). Association locations in temporal and also prefrontal cortices procedure the details of facial expressions and also face-voice combine to analyze their meaning in the ongoing socio-emotional context. The output of these locations is an important for selecting options of reciprocation and also for estimating the result of each choice. The decision is at some point reflected in the task of motor locations that manage directly the voluntary movements of the face.

Compared to the voluntary regulate of the limbs, the voluntary regulate of the confront is poorly understood. While four execute motions such as reaching and also grasping with kinematics that deserve to be precisely measured, the muscle of face expressions rearrange the construction of the facial functions to express emotions. Emotions room more difficult to quantify 보다 arm kinematics, yet even if this obstacle can be overcome, facial expressions deserve to be produced even in the absence of emotion. The dissociation in between the voluntary and emotional production of facial expressions has been amply recorded in stroke patients with damages to different motor areas. Patients with strokes in the are of the middle cerebral artery (primary motor and premotor areas) cannot create a symmetrical, voluntarily smile, nevertheless can smile typically in an answer to joke (Monrad-Krohn, 1924; Hopf et al., 1992; Dawson et al., 1994; Töpper et al., 1995; Trepel et al., 1996). This findings suggest the presence of an alternative “limbic” pathway that controls face expressions. Indeed, patients with strokes in the territory of the anterior cerebral artery, affect the midcingulate area, room able to make voluntary facial movements yet are can not to develop spontaneous emotionally expressions (amimia) (Wilson, 1924; Feiling, 1927; Karnosh, 1945).

The cortical motor areas involved in production of face expressions include: the main motor cortex, the ventrolateral premotor cortex, the supplementary engine area, and also two motor locations of the dorsal midcingulate (Morecraft et al., 2001, 2007). The localization the the two face locations in the midcingulate cortex is based upon the occupational of Vogt (2009), who determined in the cingulate cortex a subgenual, an anterior (rostral come the genu that the body callosum), and also a supracallosal section (dorsal to the body callosum). The supracallosal an ar has to be designated the midcingulate. The midcingulate has been further separated in anterior and also posterior midcingulate, which contains two premotor areas for the face: a rostral area in the anterior part of the midcingulate, designated through Morecraft et al. (2004) as M3, and also a caudal area, in ~ the border in between the anterior and also posterior departments of the midcingulate, designated together M4 through the exact same authors (Figure ​(Figure11).


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The motor control of the face. The lower fifty percent of the face is managed by the coordinated task of three motor areas: M1, primary motor cortex; PMCvl, premotor cortex ventrolateral division; and M4, caudal face area that the midcingulate cortex. The upper fifty percent of the face is managed by the coordinated activity of two motor areas: SMA, supplementary motor area; and M3, the anterior confront area the the midcingulate cortex. The black arrows indicate direct projections indigenous the basal cell nucleus of the amygdala to PMCvl, M3, M4, and SMA, The very first segment that the orange and green lines suggest the corticobulbar tract. VII, pontine facial nucleus that contain the engine neurons the synapse ~ above the muscle of face expressions. The medial department of the face nucleus consists of the engine neurons that manage muscles in that upper half of the challenge (in green) when the lateral department contains the neurons that regulate the muscles in the lower component of the face (in orange). Note that the amygdala receive multiple lines of viscerosensory input (red arrows, top) that are likely integrated in the calculation directed at facial motor areas.


The confront area of the primary motor cortex innervates engine neurons in the lateral segment of the contralateral face nucleus that manage the reduced facial muscles (Morecraft et al., 2001). The major motor cortex additionally controls the muscles affiliated in mastication and also other jaw motions that are innervated through trigeminal engine fibers.

The face area in the ventrolateral regions of the premotor cortex (PMCvl) straight innervates engine neurons in the lateral segment that the contralateral facial nucleus that regulate the reduced facial muscles (Morecraft et al., 2001). In general, the premotor cortex initiates movements triggered by external cues (Murata et al., 1997; Fogassi et al., 2001; Mushiake et al., 2006). For facial expressions the external cues can be the face expressions the others showing up to the PMCvl from temporal cortices and also the amygdala (Avendaño et al., 1983). Notably, the PMCvl area is critical for linking the perception and production the actions, a procedure thought to it is in instantiated by mirror neurons (Di Pellegrino et al., 1992; Gallese et al., 1996). A complete mirror neuron device for facial expression, akin to the winter neurons because that limb movements, has actually not to be experimentally confirmed. However, suggestive findings show that in monkeys, neurons in the ventral premotor cortex respond during the observation and execution the a particular form of face expression (Ferrari et al., 2003).

The supplementary engine cortex (SMA) straight innervates engine neurons in the medial segment the the face nucleus (medulla) that regulate the top facial muscles (Morecraft et al., 2001). Compared to the PMCvl the controls motions triggered by outside cues, the SMA appears to manage self–initiated motions (Eccles, 1982; Romo and also Schultz, 1987; Lang et al., 1994). If this division of labor holds for facial expressions, the SMA could coordinate self-initiated expressions that involve the top facial musculature (e.g., winking, scowling).

The anterior and caudal face areas of the midcingulate cortex (Picard and also Strick, 2001), designated as M3 and also M4 through Morecraft et al. (2001) present further specializations. M3 provides rise come projections that target bilaterally the medial segments of the face nucleus harboring the engine neurons the supply the top facial muscles and also the muscles that move the ear (in monkeys) (Figure ​(Figure1).1). Projections originating native M3 additionally target the reticular formation of the brainstem that consists of autonomic centers likely to become activated during emotional says (Porrino and Goldman-Rakic, 1982). M3 is in position, therefore, to coordinate both the overt (behavioral) and covert (autonomic) expression that emotions. The caudal motor area, M4, (located at the border between the anterior and also posterior midcingualte) targets the lateral regions of the face nucleus, particularly the engine neurons the supply the top lip (Morecraft et al., 2007). In theory, damage to M4 have to impair key of the contralateral top lip, a movement involved in appeasing gestures in monkeys, in laugh in humans, and in disgust in both species. Indeed, in humans, operation resection that the medial wall surface of the hemisphere that includes M4 impairs smiling. The deficits brought about by M4 damage is lacking during voluntary smiles (Hopf et al., 1992) which stands in contrast to the reduced facial weakness led to by damage to primary motor cortex or come the PMCvl. That appears, therefore, that M4 is mostly connected in the emotional control of facial expressions. This area also appears come respond come the expected reward the actions, such together looking at certain visual targets (McCoy and Platt, 2005). This is not surprising in irradiate of the substantial convergent input indigenous reward-related and also motor locations of the brain (Vogt and also Pandya, 1987; Morecraft and also Van Hoesen, 1998). Maybe the most eloquent instance of the an important role the the dorsal cingulate cortex dram in the decision come socially connect with rather is the dramatic palliation of movement and also speech in a problem known as akinetic mutism (Cairns et al., 1941). The “cingulate syndrome,” a variant of akinetic mutism contains as additional symptoms flat affect, reduced alertness, and also autonomic abnormalities (Cummings, 1993). When patients recover, lock report undamaged memory for the many requests to respond to questions and also commands and also explain their lack of responses by a finish lack that desire to interact with others. The cingulate syndrome is far-ranging because the highlights the cingulate as the site where the limbic mechanism gains accessibility to the motor device (Morecraft et al., 2007). Undoubtedly multiple information processing streams converge in the cingulate cortex: multisensory temporal and frontal locations (Baleydier and Mauguiere, 1980), ache pathways (Hutchison et al., 1999; Koyama et al., 2001; Eisenberger et al., 2003; Botvinick et al., 2005; Iwata et al., 2005), and also reward pathways (Amiez et al., 2005; Chang et al., 2013). Several aspects of impact (Critchley et al., 2003), cognitive manage (Davis et al., 2005; Rudebeck et al., 2006; Hayden and also Platt, 2007; Womelsdorf et al., 2010), and also motor manage (West and Larson, 1995; Russo et al., 2002) have actually been attributed to the cingulate cortex (reviewed by Shackman et al., 2011).


A role of the amygdala in the production of face expressions

By virtue of its substantial connectivity to intuitive association locations in the temporal and frontal cortices (Amaral et al., 1992), the primate amygdala is committed to evaluate facial expressions. While the amygdala could not be necessary for the motor elaboration of face expressions, that appears an essential for picking the expression that are most suitable for a offered social context. Monkeys and humans v bilateral lesions that the amygdala show up less reserved once encountering strangers and produce more affiliative display screens (Meunier et al., 1999; Emery et al., 2001; Adolphs, 2010; Bliss-Moreau et al., 2013). In light of this findings, that is not surprising that electric stimulation of the amygdala, and seizures originating therein, reason facial motions in both humans and also monkeys (Baldwin et al., 1954; Feindel and Penfield, 1954; Feindel, 1961; valve Buren, 1961; Gloor, 1975; Bossi et al., 1984; Hausser-Hauw and also Bancaud, 1987; Fish et al., 1993). The calculation of the amygdala might influence the an option of facial expressions due to the fact that it signal the identity, facial expression, and gaze direction of others (Leonard et al., 1985; Gothard et al., 2007; Hoffman et al., 2007; Gamer and also Büchel, 2009) or the spatu impression elicited by face stimuli (Wang et al., 2013). Throughout naturalistic social interactions a class of devoted cells become energetic in the amygdala that respond when primates fixate your gaze top top the eye of various other monkeys. A subset of this “eye cells” answers only throughout eye contact (Zimmerman et al., 2012) which improves the emotional impact of face expressions. The eye cells space unconventional in the their activity depends on the dynamic exchange that gaze between the viewer and also the separation, personal, instance the viewer interacts with. Together interplay between gaze perception and the decision to do (or not) eye-contact is analogous come the reciprocity that the society signals mediated by the cingulate cortex (Amodio and Frith, 2006). Indeed, the term of eye contact is a solid predictor of facial-expression reciprocation in monkeys (Mosher et al., 2011) and in human beings (Usui et al., 2013).

Anatomically, the amygdala develops a closed handling loop through both the anterior cingulate cortex and also with area M3 (the anterior ingredient of the midcingulate) (Morecraft et al., 2007). M3 projects to the basal and also accessory basal nuclei of the amygdala and also the basal cell nucleus of the amygdala offers rise come feedback projections to all subdivisions that the cingulate cortex (Amaral et al., 1992; Morecraft et al., 2007). The substantial interconnectivity in between the amygdala and the cingulate cortex could explain the similarity of cellular responses in these 2 areas. Neurons in the amygdala and also in the midcingulate face locations respond to the production of face expressions by surveillance the expression of self. Task in these locations becomes much more synchronous during the execution of face expressions, v neural activity in the amygdala top neural changes in the midcingulate cortex. In both areas, however, the activity of individual cells may precede or monitor the productions of facial expressions (Livneh et al., 2012). Fine-grain evaluation of the temporal relationship in between the firing rate changes and the beginning of muscular task (measured through intramuscular electromyography) have demonstrated that, at least in the amygdala, neurons respond primarily after the start of facial task (Fuglevand et al., 2012). As such, the amygdala could be responding mostly to the sensory consequences associated v the production of face expressions. This finding, in addition to the function of the amygdala in surveillance the facial expressions of others (Gothard et al., 2007) suggest a winter neuron device for facial expressions that self and of rather (Dapretto et al., 2006).


Emotion-to-motor transformation in the amygdalo-cingulate circuits

Functional predictions based on the anatomical connectivity that the amygdala and also the cingulate cortex, are gradually reinforced by neural data and also from clinical observations. Patients with motor switch syndromes (DSM V, American Psychiatric Association, 2013) are either paralyzed or create abnormal motions in the absence of damages to engine pathways. This patients show up to have a hyperactive amygdalae manifested in increased anxiety, increased galvanic skin solution and baseline cortisol, heightened vigilance, and decreased vagal ton (Voon et al., 2010). Select situation studies suggest that in this patients the task levels in the amygdala and also the motor areas are inversely connected (Kanaan et al., 2007; Voon et al., 2010).

Further evidence for emotion-to-motor change comes from brand-new research on the putative duty of visceral-somatic loops in social behavior. Since 1872, as soon as Darwin connected facial expressions to emotions and implicitly to inner states the mind circuits involved and their connectivity became better known. It has actually been proposed that decision make is strongly affected by bodily says (Damasio, 1996; Critchley and also Harrison, 2013) and these signals arise in the visceral afferents. The midcingulate and also the amygdala obtain signals indigenous the viscera via the cell core of the solitary tract and also parabrachial nuclei (Amaral et al., 1992; Craig, 2002; Khalsa et al., 2009) and also via the insula which integrates interoceptive and also exteroceptive signals, additionally projects to the amygdala and the midcingulate (Mufson et al., 1981; Vogt and Pandya, 1987; Craig, 2002). Interoceptive afferents, therefore, may modulate both the perception and also the production of face expressions. Indeed, neurons in the amygdala and also cingulate cortex discharge in phase v the cardiac and also respiratory cycle (Frysinger and Harper, 1986, 1989) and in response to stimulation of the vagal nerve (e.g., Bachman et al., 1977; Hassert et al., 2004; Conway et al., 2006). An astonishing anatomical observation around the vagus nerve highlights the function of visceral inputs because that decision making: even though the diminish axons in the vagus manage the majority of internal organs, 80% that the fibers are ascending, delivering signals from the viscera to the brain (Sengupta and also Shaker, 2005). Provided the oscillatory nature that visceral afferents (e.g., systole/diastole), it is unsurprising the the tardy of cutaneous stimuli and also emotional facial expressions has actually been shown to count on the step of the cardiac cycle (Gray et al., 2009, 2012).

While the ascending segment that the visceral-limbic and also visceral-cortical loops may affect decisions (Craig, 2002; Prinz, 2004), descending segments cause autonomic changes during the manufacturing of emotional expressions. A practical overlap in this loops might explain the concomitant visceral and also facial-motor effects reason by electrical stimulation in the amygdala and the cingulate (Pool and also Ransohoff, 1949; Baldwin et al., 1954; valve Buren, 1961; Jürgens and Ploog, 1970).

In summary, recent development in our knowledge of the neural mechanisms connected in the perception and production of facial expressions is adequate to lug facial expressions right into the theoretical framework of decision making. Several elements of current decision-making theories, such as prior distributions, probabilities, loss and also gain functions, space applicable to social transactions via face expressions. Society decision-making has currently been experiment empirically and also analyzed making use of the formalisms arisen by neuroeconomics (Sanfey et al., 2003; Hayden et al., 2007; Frith and Singer, 2008; Lee, 2008). The next major difficulty will be to incorporate facial expression in this formalisms and the visceral states that contribute to the decision process.

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Conflict of attention statement

The author declares that the research was carried out in the lack of any commercial or financial relationship that might be interpreted as a potential problem of interest.