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Individual differences in response to positive and negative stimuli: endocannabinoid-based insight on approach and avoidance behaviors.

Laricchiuta D, Petrosini L - Front Syst Neurosci (2014)

Bottom Line: Approach and avoidance behaviors-the primary responses to the environmental stimuli of danger, novelty and reward-are associated with the brain structures that mediate cognitive functionality, reward sensitivity and emotional expression.Individual differences in approach and avoidance behaviors are modulated by the functioning of amygdaloid-hypothalamic-striatal and striatal-cerebellar networks implicated in action and reaction to salient stimuli.The nodes of these networks are strongly interconnected and by acting on them the endocannabinoid and dopaminergic systems increase the intensity of appetitive or defensive motivation.

View Article: PubMed Central - PubMed

Affiliation: IRCCS Fondazione Santa Lucia Rome, Italy ; Department of Dynamic and Clinical Psychology, Faculty of Medicine and Psychology, University "Sapienza" of Rome Rome, Italy.

ABSTRACT
Approach and avoidance behaviors-the primary responses to the environmental stimuli of danger, novelty and reward-are associated with the brain structures that mediate cognitive functionality, reward sensitivity and emotional expression. Individual differences in approach and avoidance behaviors are modulated by the functioning of amygdaloid-hypothalamic-striatal and striatal-cerebellar networks implicated in action and reaction to salient stimuli. The nodes of these networks are strongly interconnected and by acting on them the endocannabinoid and dopaminergic systems increase the intensity of appetitive or defensive motivation. This review analyzes the approach and avoidance behaviors in humans and rodents, addresses neurobiological and neurochemical aspects of these behaviors, and proposes a possible synaptic plasticity mechanism, related to endocannabinoid-dependent long-term potentiation (LTP) and depression that allows responding to salient positive and negative stimuli.

No MeSH data available.


Related in: MedlinePlus

Brain circuitries that mediate approach and avoidance behaviors. Salient stimuli information from the sensory systems reaches the thalamus that in turn projects to neocortex and amygdala, first to its lateral (L) and then to central (C) and basal (B) nuclei (solid black line). The amygdala in turn projects to the hypothalamus, and directly or indirectly (via orbitofrontal cortex) to the dorsal striatum. These connections are involved in avoidance responses (solid red line). The outputs from the amygdala also reach the ventral striatum and the orbitofrontal cortex, and these connections are involved in approach responses (solid green line). The dorsal striatum receives also glutamatergic inputs (solid blue line) from neocortical and thalamic areas and dopaminergic inputs (solid yellow line) from the substantia nigra. These inputs establish synapses with striatal GABAergic cells, distinct in “direct” (dashed green line) and “indirect” (dashed red line) pathway projection neurons. Direct pathway projects to the internal globus pallidus and substantia nigra, whereas indirect pathway projects to the substantia nigra by way of the external globus pallidus and subthalamic nucleus. Also the bidirectional striatal-cerebellar network (dashed black line) is involved in the emotional and motivational processes linked to approach and avoidance.
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Figure 3: Brain circuitries that mediate approach and avoidance behaviors. Salient stimuli information from the sensory systems reaches the thalamus that in turn projects to neocortex and amygdala, first to its lateral (L) and then to central (C) and basal (B) nuclei (solid black line). The amygdala in turn projects to the hypothalamus, and directly or indirectly (via orbitofrontal cortex) to the dorsal striatum. These connections are involved in avoidance responses (solid red line). The outputs from the amygdala also reach the ventral striatum and the orbitofrontal cortex, and these connections are involved in approach responses (solid green line). The dorsal striatum receives also glutamatergic inputs (solid blue line) from neocortical and thalamic areas and dopaminergic inputs (solid yellow line) from the substantia nigra. These inputs establish synapses with striatal GABAergic cells, distinct in “direct” (dashed green line) and “indirect” (dashed red line) pathway projection neurons. Direct pathway projects to the internal globus pallidus and substantia nigra, whereas indirect pathway projects to the substantia nigra by way of the external globus pallidus and subthalamic nucleus. Also the bidirectional striatal-cerebellar network (dashed black line) is involved in the emotional and motivational processes linked to approach and avoidance.

Mentions: These novel data that implicate a cerebellar substrate for approach- and avoidance-related personality traits extend the relationship between brain areas and personality to a structure that, until now, was believed to be involved primarily in motor and cognitive functions (Oliveri et al., 2007; Torriero et al., 2007; De Bartolo et al., 2009; Foti et al., 2010; Cutuli et al., 2011; Hampe et al., 2013), much less in emotional processes (Schmahmann and Sherman, 1998; Schmahmann et al., 2007; Timmann and Daum, 2007) and even less in personality individual differences (O’Gorman et al., 2006). Anatomo-clinical analyses indicate that the cerebellum is a critical neuromodulator of intellect and mood and that the posterior vermis, the so-called limbic cerebellum, chiefly regulates emotion and affect (Schmahmann, 2004; Stoodley and Schmahmann, 2010; Stoodley et al., 2012). Impaired executive and spatial functions, language deficits, and personality changes have been described in subjects with lesions of the posterior lobe and vermis (cerebellar cognitive-affective syndrome) (Schmahmann and Sherman, 1998). MRI studies have shown structural and functional abnormalities in the cerebellum in patients with personality, anxiety, or depression disorders (Pillay et al., 1997; De Bellis and Kuchibhatla, 2006; Fitzgerald et al., 2008; Baldaçara et al., 2011a,b). This evidence implicates the cerebellum in affective processing which affects personality characteristics. Moreover, the psychopathological profiles of patients who are affected by cerebellar diseases describe them as impulsive, obsessive, hyperactive, disinhibited, and developing ruminative and stereotypical behaviors—features that affect their personality style (Schmahmann et al., 2007). Even data in healthy subjects indicate limited capacity for emotional regulation after repetitive inhibitory transcranial magnetic stimulation over the cerebellum (Schutter and van Honk, 2009). The direct reciprocal connections between the cerebellum and basal ganglia (Figure 3, dashed black line) (Hoshi et al., 2005; Bostan and Strick, 2010; Bostan et al., 2010) constitute the neuroanatomical basis for the cerebellar influence on reward-related behaviors and motivation-related information processing—functions that, until now, have been attributed only to the basal ganglia (Wise, 2004; Delgado, 2007; Palmiter, 2008). It is likely that the cerebellum accelerates the “force” with which the reward is experienced (Schmahmann et al., 2007). Cerebellar activity signals when the sensory input differs from memory-driven expectations, provides a sensory prediction error, guides exploratory drive in novel environments, allows a flexible switching among multiple tasks or alternatives, and renders functions faster and more adaptive (Restuccia et al., 2007). The cerebellum performs these functions by refining the rate, rhythm, and force of the behavior and adjusting it for given situations. Essentially, the cerebellum receives information from the cortex and basal ganglia and sends a “corrected” signal back. In particular, based on cerebellar detection of error/novelty, Ito (2008) proposed that in the motor and cognitive domains the cerebellum develops both forward and inverse models. In the forward model, the cerebellum is informed by the cortex and basal ganglia with regard to information load, plans, and intentions about the upcoming behavior and on the characteristics of the environment in which the behavior is manifested. Thus, the cerebellum develops a progressive, short-cut, anticipatory model (Wymbs and Grafton, 2009; Seidler, 2010; van Schouwenburg et al., 2010). As the behavior and cognition are repeated and the anticipatory predicted feedback is received, the cerebellum becomes increasingly accurate in its predictive capacities and allows behavior to become faster, more precise, and independent of cortical control. With successful repetitions, behavior that is governed consciously by the cerebellar forward model becomes increasingly automated and the cerebellar “inverse” model is developed. This permits rapid and skilled behavior to occur at an unconscious level. The cerebellum is constantly constructing multipairs of models that constitute a complex modular architecture for adaptively regulating motor, cognitive, and emotional material. In triggering the new mental activity, the cerebellum could warn the prefrontal cortex about the absence of internal models that match the novel information, maintain the newly generated internal models, and incorporate them into routine schemes of thought. To successfully manage novelty, the cerebellum and neocortical/subcortical areas must be co-activated. Timing, prediction, and learning properties of the cerebellum, once integrated in the circuits that are formed with the neocortex, basal ganglia, and limbic system (Figure 3), could affect the control of complex novelty-related functions (D’Angelo and Casali, 2013). Thus, this widespread two-way communication sustains basal ganglia and cerebellar involvement in motor functions and cognitive and behavioral processing. Cortico-basal-cerebellar communication may influence and sustain even processes that are linked to individual differences in approach and avoidance behaviors (Figure 3, dashed black line). The basal ganglia and cerebellum have complementary roles in facilitating motivation that sustains and reinforces personality features. The positive correlation between basal ganglia and cerebellar volumes and NS scores and the negative association between basal ganglia and cerebellar volumes and HA scores are consistent with the varying levels of engagement that subjects with various personality traits require to their subcortical circuitries. In fact, subjects who search for unfamiliar situations, make the unknown known, explore new environments, display increased tendency toward risk-taking, sensation-seeking, and immediate reward-seeking, lack inhibition, as novelty seekers do, need very rapid detection of unfamiliar events, flexible switching among tasks, alternatives, and contexts, and fast adaptation to change. All these functions heavily engage basal ganglia and cerebellum.


Individual differences in response to positive and negative stimuli: endocannabinoid-based insight on approach and avoidance behaviors.

Laricchiuta D, Petrosini L - Front Syst Neurosci (2014)

Brain circuitries that mediate approach and avoidance behaviors. Salient stimuli information from the sensory systems reaches the thalamus that in turn projects to neocortex and amygdala, first to its lateral (L) and then to central (C) and basal (B) nuclei (solid black line). The amygdala in turn projects to the hypothalamus, and directly or indirectly (via orbitofrontal cortex) to the dorsal striatum. These connections are involved in avoidance responses (solid red line). The outputs from the amygdala also reach the ventral striatum and the orbitofrontal cortex, and these connections are involved in approach responses (solid green line). The dorsal striatum receives also glutamatergic inputs (solid blue line) from neocortical and thalamic areas and dopaminergic inputs (solid yellow line) from the substantia nigra. These inputs establish synapses with striatal GABAergic cells, distinct in “direct” (dashed green line) and “indirect” (dashed red line) pathway projection neurons. Direct pathway projects to the internal globus pallidus and substantia nigra, whereas indirect pathway projects to the substantia nigra by way of the external globus pallidus and subthalamic nucleus. Also the bidirectional striatal-cerebellar network (dashed black line) is involved in the emotional and motivational processes linked to approach and avoidance.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4273613&req=5

Figure 3: Brain circuitries that mediate approach and avoidance behaviors. Salient stimuli information from the sensory systems reaches the thalamus that in turn projects to neocortex and amygdala, first to its lateral (L) and then to central (C) and basal (B) nuclei (solid black line). The amygdala in turn projects to the hypothalamus, and directly or indirectly (via orbitofrontal cortex) to the dorsal striatum. These connections are involved in avoidance responses (solid red line). The outputs from the amygdala also reach the ventral striatum and the orbitofrontal cortex, and these connections are involved in approach responses (solid green line). The dorsal striatum receives also glutamatergic inputs (solid blue line) from neocortical and thalamic areas and dopaminergic inputs (solid yellow line) from the substantia nigra. These inputs establish synapses with striatal GABAergic cells, distinct in “direct” (dashed green line) and “indirect” (dashed red line) pathway projection neurons. Direct pathway projects to the internal globus pallidus and substantia nigra, whereas indirect pathway projects to the substantia nigra by way of the external globus pallidus and subthalamic nucleus. Also the bidirectional striatal-cerebellar network (dashed black line) is involved in the emotional and motivational processes linked to approach and avoidance.
Mentions: These novel data that implicate a cerebellar substrate for approach- and avoidance-related personality traits extend the relationship between brain areas and personality to a structure that, until now, was believed to be involved primarily in motor and cognitive functions (Oliveri et al., 2007; Torriero et al., 2007; De Bartolo et al., 2009; Foti et al., 2010; Cutuli et al., 2011; Hampe et al., 2013), much less in emotional processes (Schmahmann and Sherman, 1998; Schmahmann et al., 2007; Timmann and Daum, 2007) and even less in personality individual differences (O’Gorman et al., 2006). Anatomo-clinical analyses indicate that the cerebellum is a critical neuromodulator of intellect and mood and that the posterior vermis, the so-called limbic cerebellum, chiefly regulates emotion and affect (Schmahmann, 2004; Stoodley and Schmahmann, 2010; Stoodley et al., 2012). Impaired executive and spatial functions, language deficits, and personality changes have been described in subjects with lesions of the posterior lobe and vermis (cerebellar cognitive-affective syndrome) (Schmahmann and Sherman, 1998). MRI studies have shown structural and functional abnormalities in the cerebellum in patients with personality, anxiety, or depression disorders (Pillay et al., 1997; De Bellis and Kuchibhatla, 2006; Fitzgerald et al., 2008; Baldaçara et al., 2011a,b). This evidence implicates the cerebellum in affective processing which affects personality characteristics. Moreover, the psychopathological profiles of patients who are affected by cerebellar diseases describe them as impulsive, obsessive, hyperactive, disinhibited, and developing ruminative and stereotypical behaviors—features that affect their personality style (Schmahmann et al., 2007). Even data in healthy subjects indicate limited capacity for emotional regulation after repetitive inhibitory transcranial magnetic stimulation over the cerebellum (Schutter and van Honk, 2009). The direct reciprocal connections between the cerebellum and basal ganglia (Figure 3, dashed black line) (Hoshi et al., 2005; Bostan and Strick, 2010; Bostan et al., 2010) constitute the neuroanatomical basis for the cerebellar influence on reward-related behaviors and motivation-related information processing—functions that, until now, have been attributed only to the basal ganglia (Wise, 2004; Delgado, 2007; Palmiter, 2008). It is likely that the cerebellum accelerates the “force” with which the reward is experienced (Schmahmann et al., 2007). Cerebellar activity signals when the sensory input differs from memory-driven expectations, provides a sensory prediction error, guides exploratory drive in novel environments, allows a flexible switching among multiple tasks or alternatives, and renders functions faster and more adaptive (Restuccia et al., 2007). The cerebellum performs these functions by refining the rate, rhythm, and force of the behavior and adjusting it for given situations. Essentially, the cerebellum receives information from the cortex and basal ganglia and sends a “corrected” signal back. In particular, based on cerebellar detection of error/novelty, Ito (2008) proposed that in the motor and cognitive domains the cerebellum develops both forward and inverse models. In the forward model, the cerebellum is informed by the cortex and basal ganglia with regard to information load, plans, and intentions about the upcoming behavior and on the characteristics of the environment in which the behavior is manifested. Thus, the cerebellum develops a progressive, short-cut, anticipatory model (Wymbs and Grafton, 2009; Seidler, 2010; van Schouwenburg et al., 2010). As the behavior and cognition are repeated and the anticipatory predicted feedback is received, the cerebellum becomes increasingly accurate in its predictive capacities and allows behavior to become faster, more precise, and independent of cortical control. With successful repetitions, behavior that is governed consciously by the cerebellar forward model becomes increasingly automated and the cerebellar “inverse” model is developed. This permits rapid and skilled behavior to occur at an unconscious level. The cerebellum is constantly constructing multipairs of models that constitute a complex modular architecture for adaptively regulating motor, cognitive, and emotional material. In triggering the new mental activity, the cerebellum could warn the prefrontal cortex about the absence of internal models that match the novel information, maintain the newly generated internal models, and incorporate them into routine schemes of thought. To successfully manage novelty, the cerebellum and neocortical/subcortical areas must be co-activated. Timing, prediction, and learning properties of the cerebellum, once integrated in the circuits that are formed with the neocortex, basal ganglia, and limbic system (Figure 3), could affect the control of complex novelty-related functions (D’Angelo and Casali, 2013). Thus, this widespread two-way communication sustains basal ganglia and cerebellar involvement in motor functions and cognitive and behavioral processing. Cortico-basal-cerebellar communication may influence and sustain even processes that are linked to individual differences in approach and avoidance behaviors (Figure 3, dashed black line). The basal ganglia and cerebellum have complementary roles in facilitating motivation that sustains and reinforces personality features. The positive correlation between basal ganglia and cerebellar volumes and NS scores and the negative association between basal ganglia and cerebellar volumes and HA scores are consistent with the varying levels of engagement that subjects with various personality traits require to their subcortical circuitries. In fact, subjects who search for unfamiliar situations, make the unknown known, explore new environments, display increased tendency toward risk-taking, sensation-seeking, and immediate reward-seeking, lack inhibition, as novelty seekers do, need very rapid detection of unfamiliar events, flexible switching among tasks, alternatives, and contexts, and fast adaptation to change. All these functions heavily engage basal ganglia and cerebellum.

Bottom Line: Approach and avoidance behaviors-the primary responses to the environmental stimuli of danger, novelty and reward-are associated with the brain structures that mediate cognitive functionality, reward sensitivity and emotional expression.Individual differences in approach and avoidance behaviors are modulated by the functioning of amygdaloid-hypothalamic-striatal and striatal-cerebellar networks implicated in action and reaction to salient stimuli.The nodes of these networks are strongly interconnected and by acting on them the endocannabinoid and dopaminergic systems increase the intensity of appetitive or defensive motivation.

View Article: PubMed Central - PubMed

Affiliation: IRCCS Fondazione Santa Lucia Rome, Italy ; Department of Dynamic and Clinical Psychology, Faculty of Medicine and Psychology, University "Sapienza" of Rome Rome, Italy.

ABSTRACT
Approach and avoidance behaviors-the primary responses to the environmental stimuli of danger, novelty and reward-are associated with the brain structures that mediate cognitive functionality, reward sensitivity and emotional expression. Individual differences in approach and avoidance behaviors are modulated by the functioning of amygdaloid-hypothalamic-striatal and striatal-cerebellar networks implicated in action and reaction to salient stimuli. The nodes of these networks are strongly interconnected and by acting on them the endocannabinoid and dopaminergic systems increase the intensity of appetitive or defensive motivation. This review analyzes the approach and avoidance behaviors in humans and rodents, addresses neurobiological and neurochemical aspects of these behaviors, and proposes a possible synaptic plasticity mechanism, related to endocannabinoid-dependent long-term potentiation (LTP) and depression that allows responding to salient positive and negative stimuli.

No MeSH data available.


Related in: MedlinePlus