Basal-ganglia 'Projections' to the Prefrontal Cortex of the Primate

“Likewise, the GPi dominates medial premotor cortex (areas F3/SMA and F6/pre-SMA) (Akkal et al. 2007) but there is a broad crossover region of dorsal premotor and prefrontal cortex where areas such as F2/PMd and 9 receive relays from both GPi and SNr (Middleton and Strick 2002; Saga et al. 2011).”

“…et al., 2013; Pastalkova et al., 2008; Powell and Redish, 2014; Schoenbaum and Eichenbaum, 1995), which may be implemented using positive feedback through distributed cortico-striato-thalamic loops (Alexander et al., 1986; Houk and Wise, 1995; Middleton and Strick, 2000, 2002; Wang, 2001).”

“These studies showed that the amount of territory associated with prefrontal areas in GPi is comparable to the amount of volume occupied by projection neurons directed to the premotor and motor cortices through the thalamus [reviewed in Middleton and Strick (1994, 2000, 2002)].”

“These cortical regions all project to the striatum (Haber et al., 2006), and they also receive input from the basal ganglia through basal ganglia-thalamocortical pathways (Middleton and Strick, 2002).”

“Most likely, this is mediated by the connectivity with the prefrontal cortex (eg., Alexander and Crutcher, 1990; Di Martino et al., 2008; Draganski et al., 2008; Hoover and Strick, 1993;Middleton and Strick, 2002).”

“, 1982), as well as indirect effects of striatal dopamine loss on the function of downstream nodes of the cortico-striato-pallido-thalamocortical (CSPTC) loops and related pathways (Carbon et al., 2003; Middleton and Strick, 2002; Wichmann and DeLong, 1996).”

“One major target of this efferent pathway is the frontal cortex (Middleton and Strick 2002).”

“…is an integral component of a corticostriatal circuit involved in motivated behaviors (Haber & Knutson, 2010; Balleine, Delgado, & Hikosaka, 2007; Middleton & Strick, 2002; Alexander & Crutcher, 1990), with important connections with cortical regions, such as OFC and ACC (Haber & Knutson, 2010).”

“It has been shown that there is an intricate neuroanatomical correlation between PFC and the basal ganglia (mainly the striatum)[21].”

“Strick and colleagues championed intracerebral injection of HSV as a means of defining multisynaptic circuits in primate brain (Zemanick et al., 1991; Hoover and Strick, 1993, 1999; Middleton and Strick, 2001, 2002).”

“The strong connections between the PFC and the basal ganglia as seen in animal (Maurice et al., 1998, 1999; Middleton and Strick, 2002) and human studies (Voytek and Knight, 2010) may be responsible for activation in these deeper regions of cortex following PFC stimulation.”

“This work suggests that the entirety of the dorsal striatum can contribute, in some circumstances (see also Miyoshi et al., 2012), to navigational behaviors which also draw upon spatial mapping mechanisms.”

“This dopamine depletion impacts the functioning of four rontostriatal circuits involved in different motor, cognitive, affecive, and motivational aspects of behavior [5,22,50,70].”

“However, recent advances in restingstate fMRI connectivity analysis and in polysynaptic anatomical tracing find evidence for fine-scale specificity in cortico–cerebellar networks similar to the specificity observed in cortico-striatal networks [9 ,10 ,18 ,75].”

“…establishing that basal ganglia and thalamus, through their interaction with cortex, are involved in a wide range of other functions, coordinating sensorimotor, limbic, and cognitive systems (Cohen and Frank, 2009; Middleton and Strick, 2000, 2002; Seger, 2006, 2008; Seger and Spiering, 2011).”

“More precisely, prSN is connected with the motor cortex, temporal cortex (TE), prefrontal eye field (BA 8), and prefrontal cortex (BA 9/12/46) in monkeys.(47,48) Our in vivo human study confirms these previous observations and shows that these circuits are clearly identifiable during the brain resting state, though it…”

“Our results are in line with previous data on axonal tracing of cortico-striatal (Inase et al., 1996; Middleton and Strick, 2002; Ongur and Price, 2000; Selemon and Goldman-Rakic, 1988), striato-pallidal and striato-nigral (Hazrati and Parent, 1992; Parent et al., 1984) projection studies.”

“…has been linked to planning, as seen using the Tower of London paradigm (Beauchamp et al., 2003; Dagher et al., 1999; Rowe et al., 2001; van den Heuvel et al., 2003) and when planning new response strategies during a variation on the Wisconsin Card Sorting Test (Monchi et al., 2001, 2006).”

“Studies using this technique identified finer connectivity patterns between specific cortical areas, such as projections from specific sub-regions of the BG to the motor and association cortices (Middleton and Strick, 1994, 2000b, 2002; Kelly and Strick, 2004; Akkal et al., 2007; Saga et al., 2011).”

“Of particular importance in the context of the frontal lobe is the cortico-basal ganglia neural circuit that interconnects mainly prefrontal areas to the basal ganglia [18,19,20,21,22,23,24,25,26] and is functionally associated to elements of ‘executive control’: control and selection of actions [27]; guidance of rewa…”

“…Price, 1994; Deschênes et al., 1996; Tsumori et al., 2002), the SNr neurons convey the striatal outflow to motor, premotor, prefrontal, and associative sensory cortical areas (Parent, 1990; Deniau and Chevalier, 1992; Middleton and Strick, 1996, 2002; Sakai et al., 1998; Mailly et al., 2003).”

“For instance, because the SNr is strongly involved in associative and limbic basal ganglia circuits (Haber and Fudge 1997; Middleton and Strick 2002; Parent and Hazrati 1994), some of the cognitive or emotional side effects of D1LR-active drugs may be mediated through activation of the nigral…”

“The premotor cortex receives input from the basal ganglia (Middleton and Strick 2002), and classical rate-theory models of PD pathophysiology would suggest that overactivity in basal ganglia output nuclei would reduce activity in cortical targets (DeLong 1990).”

“In addition, the basal ganglia also has strong connections to the cingular cortex (Middleton and Strick, 2002).”

“Pre-SMA belongs to the prefrontal cortex because of its extensive connections with most prefrontal areas (46, 8A, 9, 10, 11, 12 and 13) (Inase et al., 1999; Middleton and Strick, 2002).”

“…knowledge, the first such demonstration in the context of postural control, but it is not entirely surprising since it is known that there are closed loops between the structures of the basal ganglia and various cortical areas involved in posture control (Middleton and Strick, 1996, 1997, 2002).”

“Although their modelling work to date has been confined to motor-cortical selection (Prescott, et al., 2006), the anatomical structures and pathways they have emulated seem to be replicated for much of the cortical sheet (Alexander, et al., 1986; Middleton & Strick, 2002; Postuma & Dagher, 2006).”

“Of high importance, PFC plays a pivotal role, since it receives projections from both motor and sensory areas that are crucial for learning and is an intricate neuroanatomical correlation [44].”

“…along with the well-established structural connections between frontal and subcortical structures (e.g., Alexander, Delong, & Strick, 1986; Middleton & Strick, 2000), we endeavored to use functional magnetic resonance imaging (FMRI) to examine neural activity in frontal-subcortical…”

“…functions, regulated by catecholamine systems (Arnsten and Li, 2005), involve distinctive brain areas, including the prefrontal cortex, thalamus, basal ganglia, cerebellum and parietal and temporal lobes (Middleton and Strick, 2001, 2002; Collette and Van der Linden, 2002; Willcutt et al., 2005).”

“…regional heterogeneity in the degree of cortical atrophy and the cortical laminae involved (Heinsen et al., 1994; Macdonald et al., 1997; Passani et al., 1997), and recent analysis of regional cortical thinning in HD patients at different stages of the illness showed that there is a…”

“Retrograde axonal tracing studies in primates have shown that the DLPFC, including BA9, is an integral part of the cortico-basal gangliathalamocortical circuit (Reviewed in Middleton and Strick 2002).”

“…which receive converging inputs in the supra-granular layers and send top-down outputs via columnar connections with sub-granular layers to dorsal striatum (caudate nucleus and putamen) to provide parallel cortico-striatal-thalamo-cortical loops 6,9,14,15 for different types of sensory inputs.”

“Furthermore, these portions have © 2015 Federation of European Neuroscience Societies and John Wiley & Sons Ltd European Journal of Neuroscience, 43, 258–269 been shown to project to the PMd (Saga et al., 2011), as well as to the prefrontal cortex (Middleton & Strick, 2002), across synapses.”

“Macaques are useful as developmental models because nonhuman primate cortical structures are similar to humans in the frontal cortical and striatal regions important in ADHD (Mostofsky et al, 2002; Sowell et al, 2003) and are shown to mediate psychomotor and executive function (Haber, 2003; Middleton and Strick, 2002).”

“Not only Patient with migraine Electric stim alone do the thalamo-cortical loops regulate the excitability of sensory cortices but they also set the activation of excitatory and inhibitory interneurons in the motor cortices (Middleton and Strick, 2002).”

“Retrograde virus tracing studies have shown that the output projections of the basal ganglia reach multiple cortical areas implicated in the control of both motor and cognitive functions (Hoover and Strick 1993, 1999; Middleton and Strick 2000, 2002).”

“Based on neurophysiological models and anatomical data, it is assumed that there are both parallel (Alexander et al., 1990; Middleton and Strick, 2002) and converging pathways in corticobasal ganglia loops (Takada et al.”

“Many studies have demonstrated the involvement of the basal ganglia nuclei in higher-level cognition due to its participation in habit learning and other procedural processes (White 1997; Graybiel 1998; Middleton and Strick 2000; Middleton and Strick 2002; Fuji and Graybiel 2005).”

“Several different models for this circuit were proposed, starting from the classical box-and-arrow AlbinDeLong model (8,9), through the example of parallel processing of cortical information (10).”

“Cerebral Cortex May 2011;21:1084--1093 doi:10.1093/cercor/bhq182 Advance Access publication September 23, 2010”

“Both CDt and cvPut are known to receive direct inputs from the temporal cortex (55) and send signals indirectly to the temporal cortex (56) and the prefrontal cortex (57).”

“The factor “group” was significant both for TDT [F(1,16) Table Demographic and clinical information on the patients with”

“In the brain, the selection of goals strongly relies on PFC (Miller and Cohen, 2001) forming re-entrant connections with BG, in particular the nucleus accumbens portion of striatum (NAcc; Middleton and Strick, 2002; Haber, 2003).”

“Dorsal striatum receives inputs from structures involved in expressing instrumental behaviors, which feed back to their point of origin in the frontal lobes (Middleton and Strick, 2000; Middleton and Strick, 2002).”

“DLPFC, which in PD shows more variable degree of dopaminergic loss, receives projections both from the caudate [25] and the ventral tegmental area (VTA) [26].”

“Thus, through efferents to basal ganglia and motor cortex, prefrontal ensembles appear well suited to organize goal-directed action sequences (Sesack et al., 1989; Gu et al., 1999; Middleton and Strick, 2002; Dum and Strick, 2005).”

“, BA 4, S1; Kunzle, 1975, 1977] to frontal lobe areas, including SMA and prefrontal areas [Alexander et al., 1986; Middleton and Strick, 2002].”

“The frontal cortex receives the largest portion of BG outputs (via the thalamus), suggesting a close collaboration between the BG and frontal cortex.(23,24) DA acts not only on the PFC but also on the BG.”

“Projections then arise from the respective areas of the thalamus back to the DLPFC, thus completing the circuit (Bonelli and Cummings, 2007; Middleton and Strick, 2002).”

“…and DS are heavily interconnected with multiple cortical and subcortical regions, including the orbitofrontal and ventromedial prefrontal cortex, anterior cingulate cortex, amygdala, thalamus, and anterior insula (Middleton and Strick, 2002; Reynolds and Zahm, 2005; Wright and Groenewegen, 1996).”

“Indeed, hand-related neural activity was recorded even rostral to themicroexcitablemotor putaminal region, likely in the location of the rostral grasping zone (Crutcher and DeLong 1984; Alexander and DeLong 1985).”

“…motor and executive corticobasal ganglia loops that have been described in humans and monkeys (Haber, 2003; Haber and Behrens, 2014; Haber et al., 2006; Haber and Knutson, 2010; Middleton, 2000; Middleton and Strick, 2002; Nambu, 2011; Parent, 1990; Parent et al., 1995; Postuma and Dagher, 2006).”

“These include motor, oculomotor, limbic, and associative circuits, which are thought to remain segregated throughout their subcortical course (see, e.g., Middleton and Strick 2002 for a recent review).”

“In turn the GPi projects via the ventral thalamus to the both the anterior and posterior sectors of dorsal PMc (Inase & Tanji, 1994; Kurata, 1994) as well as to ventral PMc, motor cortex and other frontal areas (Middleton & Strick, 2000, 2002).”

“…by guest on 04 June 2021 tracings, have clearly demonstrated that both the basal ganglia and cerebellum have extensive reciprocal connections with association cortices, including various regions of the prefrontal cortex (Middleton & Strick, 2001, 2002).”

“The VA nucleus is connected with prefrontal as well as premotor areas (Kievit and Kuypers 1977; Jacobson et al. 1978; Kunzle 1978; Baleydier and Mauguiere 1980; Ilinsky et al. 1985; Asanuma et al. 1985; Goldman-Rakic and Porrino 1985; Preuss and Goldman-Rakic 1987; Yeterian and Pandya 1988; Barbas et al. 1991; Chiba e…”

“1A) is primarily based on prior animal studies (Alexander and Crutcher, 1990; Haber et al., 2000; Middleton and Strick, 2002; Voorn et al., 2004; McHaffie et al., 2005).”

“The prefrontal territory within the GPi was seen to comprise one third of the total GPi volume (Middleton and Strick, 2002) and was located within the anterior and dorsal GPi section (Middleton and Strick, 2002; Yoshida et al., 1993).”