So how does the neocortex communicate with the subcortical corpus striata complex? In "Frontal-Subcortical Circuits and Human Behavior" (1993), Jeffrey L. Cummings explains:
Five circuits are currently recognized: a motor circuit originating in the supplementary motor area, an oculomotor circuit with origins in the frontal eye fields, and three circuits originating in prefrontal cortex (dorsolateral prefrontal cortex, lateral orbital cortex, and anterior cingulate cortex). The prototypic structure of all circuits is an origin in the frontal lobes, projection to striatal structures (caudate, putamen, and ventral striatum [includes nucleus accumbens]), connections from striatum to globus pallidus and substantia nigra, projections from these two structures to specific thalamic nuclei, and a final link back to the frontal lobe. Within each of the circuits there are two pathways: (1) a direct pathway linking the striatum and the globus pallidus interna/substantia nigra complex and (2) an indirect pathway projecting from striatum to globus pallidus externa, then to subthalamic nucleus, and back to the globus pallidus interna/substantia nigra. Both direct and indirect circuits project to the thalamus. All circuits share common structures—frontal lobe, striatum, globus pallidus, substantia nigra, and thalamus—and are contiguous but remain anatomically segregated throughout. Projections are progressively focused onto a smaller number of neurons as they pass from cortical to subcortical structures, but circuit segregation is maintained. There are open and closed aspects to the circuits; structures receive projections from noncircuit cortical areas, thalamus, or amygdaloid nuclei and project to regions outside the circuits. Structures projecting to or receiving projections from specific circuits are anatomically and functionally related. The circuits focus input on restricted cortical targets; several cortical regions project to the striatum, where the output is funneled through sequential circuit structures to limited frontal lobe areas.
To see a diagram of how the cortical-subcortical circuits are organized, including the direct pathway (labeled A - RELEASE) and the indirect pathway (labeled B - INHIBIT) mentioned above, link here to the American Journal of Psychiatry. We will discuss the commentary provided with the graphic and photograph in the paragraphs below. Source: Images in Neuroscience, Carol A. Tamminga, M.D., Editor, Am J Psychiatry 158:1, January 2001.
Regarding the American Journal of Psychiatry graphic mentioned above, it is embeded in this webpage, the GABA neurosignaling originates, at least in part, from the nucleus accumbens. As the graphic illustrates, GABA neurosignaling is of extreme importance in managing motor output—both in releasing motor activity and inhibiting motor activity. We will discuss this in greater detail below.
Because this subject is so complex, an excerpt from C.M.A. Pennartz et al., "Corticostriatal Interactions During Learning, Memory Processing, and Decision Making" (2009), is included here. Remember that pallidum is another term for globus pallidus.
Cortical projections to the striatum are topographically ordered in a series of parallel anatomical "loops" running from neocortex to the striatum, pallidum, thalamus, and back to neocortex. These parallel macrocircuits have been linked to different global functions: whereas a "limbic," ventromedial prefrontal [cortex]–ventral striatal loop has been delineated to mediate motivational and reward processing, other loops engage in sensorimotor or cognitive processing (Alexander et al., 1990 ; Graybiel et al., 1994 ; Voorn et al., 2004 ; Yin and Knowlton, 2006 ). Information processed along these pathways is under the modulatory control of dopamine released from fibers originating in the ventral tegmental area (VTA) and substantia nigra pars compacta (SNpc). Given the parallel organization of corticostriatal circuits, the question arises how coherent behavior, requiring integration of sensorimotor, cognitive, and motivational information, is achieved.
In other words, coherent behavior is produced when these parallel circuits somehow share information. This brings us back to Suzanne N. Haber's article, "The Primate Basal Ganglia: Parallel and Integrative Networks" (2003), which we discuss above. Haber writes: "Recent anatomical evidence from primates demonstrates that the neuro-networks within basal ganglia pathways are in a position to move information across functional circuits."
Is the nucleus accumbens an actuator?
The nucleus accumbens shell has a high density of dopamine (D1 and D3) receptors. Jaak Panksepp's observation in Affective Neuroscience bears repeating. He notes that the overall functions of the basal ganglia [corpus striata including nucleus accumbens] "are under the control of one major 'power switch'—ascending brain dopamine." Neurons in the ventral tegmental area (VTA) project, via the mesolimbic pathway, directly to the nucleus accumbens, where they release dopamine—one aspect of the ascending brain dopamine to which Panksepp refers. If you remember from material in Part 2 of CorticalBrain.com, Panksepp concludes that the mesolimbic dopamine pathway and the mesocortical dopamine pathway are essential components of the SEEKING system, which directs our search for resources and solutions. (See Dopamine action, synthesis, and pathways and The Brain's SEEKING System.)
To emphasize the importance of the nucleus accumbens as a link between the brain's emotive center (the hippocampi and amygdalae), motivational center (dopamine-producing neurons in the VTA in the midbrain), and motor center (dopamine-producing neurons in the substantia nigrae), it is quoted more directly from the scientists who have studied the nucleus accumbens. In a 1983 The Journal of Neuroscience study titled "Neural Projections from Nucleus Accumbens to Globus Pallidus, Substantia Innominata, and Lateral Preoptic- Lateral Hypothalamic Area: An Anatomical and Electrophysiological Investigation in the Rat," G.J. Mogenson, L.W. Swanson, and M.Wu conclude: Since the nucleus accumbens receives substantial inputs from the hippocampal formation (Swanson and Dowan, 1977) and the amygdala (Krettek and Price, 1978; Newman and Winans, 1980), this evidence has led to the suggestion that it may serve as an important link between the limbic system on the one hand and somatomotor control systems on the other (Swanson and Cowan, 1975; Mogenson et al., 1980; Swanson and Mogenson, 1981).
The way It is conceptualized motivated behavior in humans—being careful not to confuse motivation with will—is thus: the nucleus accumbens receives dopamine SEEKING signaling from neurons in the VTA along with emotionally-tagged VIGILANCE signaling from the amygdala and hippocampus. So what is the purpose of the nucleus accumbens? It is proposed that the nucleus accumbens may serve as an actuator, which the Princeton University WordNet defines as "a mechanism that puts something into automatic action." Such a function would ensure that, upon perceiving a threat, an animal could respond almost automatically with a bioprogramed sequence of behavior. Here, the term bioprogram refers to either 1) an innate neural firing pattern created via evolution that, like fixed-action patterns, involves specific movements and sequence, or 2) a learned pattern of neural activity that has been kindled to perform something like an innate bioprogram, or 3) a combination of innate and learned neural activity that have interdigitated over time through kindling. It is conceptualized that this third kind of bioprogram as being responsible for some post-traumatic stress symptoms. Think of the drills and routines soldiers learn in order to respond to threat. Once back at home in peaceful surroundings, those learned responses do not just vanish. And if a stimulus pops up unexpectedly—for example, a car backfiring—one might be forced to find a way to suppress behavior that, if acted out, would be inappropriate to one's environment. Having to do something to release surging motivation, one might engage in a displacement activity. In other words, symptoms would emerge. For a review, see Displacement, stereotypies, frustration, and perseveration—understanding ADHD, OCD, PTSD, and Tourette syndrome.
Even in times of threat, when an automated response helps ensure survival, the response cannot stay "on" forever. An animal or human would never get rest. This is where gamma-aminobutyric acid (GABA) comes in.
The Wikipedia image directly to the left(links to source) represents the chemical structure of gamma-aminobutyric acid (GABA). For details on GABA, see the Scholarpedia entry, which Eugene Roberts, who discovered GABA, curates. Click on the photograph of Roberts below right to read his biography.
In their abstract presented below from "Nucleus accumbens to globus pallidus GABA projection subserving ambulatory activity" (1980), D.L. Jones and G.J. Mogenson suggest that the nucleus accumbens releases gamma-aminobutyric acid (GABA) into the globus pallidus to attenuate motor activity. Thus, the GABA may be serving as a sort of "off" signal to the globus pallidus, which as we have discussed, is deeply recessed within the corpus striata complex and is an integral component in cortical-subcortical parallel circuits.
The Merck Manuals Online Medical Library explains that GABA is "the major inhibitory neurotransmitter in the brain. … After interaction with its receptors, GABA is actively pumped back into nerve terminals and metabolized." In the Jones and Mogenson study, when the authors blocked GABA with picrotoxin, motor activity increased. When they injected GABA into the system, motor activity decreased. So while dopamine input to the nucleus accumbens is certainly the "on" switch in the SEEKING system, it looks like GABA could be an "off" switch of sorts. When levels of either neurochemical are out of balance, during the integration of emotive, motivational, and motor neurosignaling, motor dysfunction could result. Jones and Mogenson write:
The present experiments investigated the hypothesis of a projection relating to the release of gamma-aminobutyric acid (GABA) from the nucleus accumbens to the globus pallidus subserving ambulatory activity in the rat. The GABA antagonist picrotoxin, microinjected into the globus pallidus, elicited dose-dependent increases in ambulatory activity. The administration of dopamine into the nucleus accumbens had a synergistic effect and further stimulated ambulatory activity. GABA injected into the ventral posterior globus pallidus significantly attenuated the ambulatory activity stimulated by injecting dopamine into the nucleus accumbens. These observations provide evidence of a GABAergic projection from the nucleus accumbens to the globus pallidus and implicate it in the initiation of ambulatory activity.
As a last note before leaving this subsection on the nucleus accumbens, it is noted here that later in Part 3 of CorticalBrain.com, we will discuss the successful use of deep-brain stimulation to the nucleus accumbens as a treatment for obsessions and compulsions.
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