Inputs to the Dorsal Striatum of the Mouse Reflect the Parallel Circuit Architecture of the Forebrain

“The profound effects of pathological disruptions have indicated a critical role for the processing of excitatory input within the striatum (Albin et al., 1989).”

“The topographical organization of inputs to and outputs from the striatum has long played a central role in both theory and the interpretation of functional data in the basal ganglia (Ragsdale and Graybiel, 1990; Mink, 1996).”

“However, while projections from the amygdala to the ventral striatum have indeed received quite a lot of attention (Gray, 1999; Cardinal et al., 2002; Floresco et al., 2008; Belin et al., 2009; Humphries and Prescott, 2010), the projections to the dorsal striatum that were observed with anterograde…”

“These recent behavioral results have shed light on the critical and specific roles of the dorsal striatum in instrumental conditioning and motor control that complement and extend earlier ideas about roles of striatal subregions in modality specific learning (Graybiel et al., 1994; Packard and Knowlton, 2002).”

“Given the critical requirement of the dorsal striatum in the acquisition and expression of goal-directed instrumental conditioning and the central role that error prediction signals are thought to play in such learning (Schultz, 2006), the amygdalostriatal projection may be an important component of an extended learni…”

“Based upon retrograde and anterograde labeling in the primate it has been previously suggested that dopaminergic neurons may play a critical role in transferring information between the medial and lateral striatum (Haber et al., 2000; Haber, 2003).”

“…an apparent minority of the labeling, the zones of overlap may be disproportionately important to the function of the dorsolateral striatum in the rat (Brown and Sharp, 1995), as has been proposed in the primate (Graybiel et al., 1994; Haber, 2003; Cohen and Frank, 2009; Haber and Calzavara, 2009).”

“An important support for this model was a series of elegant studies in the monkey that revealed a convergence of functionally related, but anatomically distant, neocortical regions (Flaherty and Graybiel, 1991, 1995; Parthasarathy et al., 1992; Parthasarathy and Graybiel, 1997).”

“Indeed, it has recently been demonstrated that activity in the amygdala is highly correlated with learning and reflects both value and error prediction signals that are tightly correlated with learning (Paton et al., 2006; Belova et al., 2008).”

“Our labeling was consistent with early studies in which injection of tritiated amino acids into the CEA and BLA revealed labeled axons across a large extent of the dorsal striatum in the rat (Kelley et al., 1982; Price, 1986).”

“The projection of serotonergic neurons to the dorsal striatum has received some attention (Di Matteo et al., 2008), especially interesting due to its proposed role in mediating opponent learning (Daw et al., 2002; Doya, 2008).”

“It was observed in the earliest tract tracing studies that axons from subregions and lamina of the neocortex were inhomogeneously distributed in the dorsal striatum of rats (Gerfen, 1984) or the caudate–putamen (CPu) of primates (Goldman and Nauta, 1977).”

“More recently, an analogous dissociation between the dorsomedial and dorsolateral striatum during motor learning has also been demonstrated in mice (Yin et al., 2009).”

“Scale bars: 1 mm. Frontiers in Neuroanatomy www.frontiersin.org December 2010 | Volume 4 | Article 147 | 10 surface of the SNr – a position consistent with the localization of the VTA (Figure 5).”

“Although it has received less attention as an important axis of functional differentiation, recent results suggest that the anterior and posterior striatum have dissociable behavioral effects (Tricomi et al., 2009; Shiflett et al., 2010).”

“…an apparent minority of the labeling, the zones of overlap may be disproportionately important to the function of the dorsolateral striatum in the rat (Brown and Sharp, 1995), as has been proposed in the primate (Graybiel et al., 1994; Haber, 2003; Cohen and Frank, 2009; Haber and Calzavara, 2009).”

“The projection of serotonergic neurons to the dorsal striatum has received some attention (Di Matteo et al., 2008), especially interesting due to its proposed role in mediating opponent learning (Daw et al., 2002; Doya, 2008).”

“In the thalamus we reliably observed retrograde labeling of neurons not only in the parafascicular (PF) and centromedian (CM) intralaminar nuclei (Smith et al., 2004), but also within sensory nuclei located more laterally such as the posterior (PO), ethmoid (Eth), medial (MG), and lateral…”

“It has been elegantly demonstrated in rats that a profound dissociation between goaldirected and habitual behavior could be mapped onto circuits in the dorsomedial (Yin et al., 2005a,b) and dorsolateral striatum (Yin et al., 2006), respectively.”

“Although future experiments will be required to determine whether such a “spiral” structure is present in the rodent brain (Yin et al., 2008; Belin et al., 2009), our data are consistent with a topographical organization that could subserve a similar function.”

“It was observed in the earliest tract tracing studies that axons from subregions and lamina of the neocortex were inhomogeneously distributed in the dorsal striatum of rats (Gerfen, 1984) or the caudate–putamen (CPu) of primates (Goldman and Nauta, 1977).”

“…labeled neurons appeared distributed throughout a wider range of cortical layers extending from the border of layer III to layer VI (Figure 3); reminiscent of the broad laminar distribution corticostriatal neurons identified with anterograde tracing in the frontal cortex of the rat (Gerfen, 1989).”

“…to the ventral striatum have indeed received quite a lot of attention (Gray, 1999; Cardinal et al., 2002; Floresco et al., 2008; Belin et al., 2009; Humphries and Prescott, 2010), the projections to the dorsal striatum that were observed with anterograde tracing in the rat (Kelley et al., 1982),…”

“Although future experiments will be required to determine whether such a “spiral” structure is present in the rodent brain (Yin et al., 2008; Belin et al., 2009), our data are consistent with a topographical organization that could subserve a similar function. the cortIcostrIatal Pathway Finally,…”

“Despite deep similarities in the anatomy of the basal ganglia in vertebrates, significant differences are nonetheless present (Reiner et al., 1998).”

“In addition, elegant single cell labeling studies have discovered a feedback pathway from the GP to the striatum (Bevan et al., 1998).”

“…extent and importance of functional convergence is unclear in rats, and unknown in mice, in the last several years it has become clear that anatomically distinct regions of the striatum have dissociable functional properties (Packard and Knowlton, 2002; Balleine et al., 2009 Redgrave, 2010 #256).”

“This is also the case in the primate, but an elegant series of studies demonstrated a robust convergence of functionally related sensory and motor structures in the striatum despite this separation along the anterior–posterior axis (Ragsdale and Graybiel, 1990; Parthasarathy et al., 1992; Flaherty and Graybiel, 1995;…”

“…and DeAmicis, 1977; Hersch and White, 1982; Porter and White, 1983; Bernardo and Woolsey, 1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al., 2003; Miura et al., 2007; Brazhnik et al., 2008; Usunoff et al., 2009; Ibáñez-Sandoval et al., 2010; Tlamsa and Brumberg, 2010) and to…”

“…while projections from the amygdala to the ventral striatum have indeed received quite a lot of attention (Gray, 1999; Cardinal et al., 2002; Floresco et al., 2008; Belin et al., 2009; Humphries and Prescott, 2010), the projections to the dorsal striatum that were observed with anterograde…”

“The PO nucleus receives primary sensory afferents from brainstem nuclei (Paxinos, 2004) and the Eth nucleus additionally receives feedback from the motor cortex via zona incerta (Barthó et al., 2002).”

“However, even though we selected fluorescent beads for their useful property minimal diffusion away from the injection site and uptake by actively cycling axon terminals (Vercelli et al., 2000), it is still difficult to precisely identify the site of injection and to rule out a biased diffusion or in homogeneous uptak…”

“…an apparent minority of the labeling, the zones of overlap may be disproportionately important to the function of the dorsolateral striatum in the rat (Brown and Sharp, 1995), as has been proposed in the primate (Graybiel et al., 1994; Haber, 2003; Cohen and Frank, 2009; Haber and Calzavara, 2009).”

“In the rat sensory and motor projections to the striatum are only partially overlapping (Hoffer and Alloway, 2001; Alloway et al., 2006) even though sensory and motor areas at the same position in the anterior–posterior axis may converge more substantially (Ramanathan et al., 2002).”

“Yet, despite the substantial literature on the vertebrate striatum, there have been relatively few anatomical studies of the macrocircuitry of the mouse (White and DeAmicis, 1977; Hersch and White, 1982; Porter and White, 1983; Bernardo and Woolsey, 1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al…”

“Indeed, it has recently been demonstrated that activity in the amygdala is highly correlated with learning and reflects both value and error prediction signals that are tightly correlated with learning (Paton et al., 2006; Belova et al., 2008).”

“This is also the case in the primate, but an elegant series of studies demonstrated a robust convergence of functionally related sensory and motor structures in the striatum despite this separation along the anterior–posterior axis (Ragsdale and Graybiel, 1990; Parthasarathy et al., 1992; Flaherty and Graybiel, 1995;…”

“In addition, anterograde tracing has demonstrated that the topographic organization of the striatum is maintained in a more compact form at its output targets in the ventral midbrain (Tulloch et al., 1978; Deniau et al., 2007).”

“Careful registration of labeling patterns across subjects and the development of techniques for simultaneous use of multiple labels provided clear evidence for a topographical organization of the corticostriatal projection (Malach and Graybiel, 1986; Gerfen, 1992).”

“The projection of serotonergic neurons to the dorsal striatum has received some attention (Di Matteo et al., 2008), especially interesting due to its proposed role in mediating opponent learning (Daw et al., 2002; Doya, 2008).”

“…1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al., 2003; Miura et al., 2007; Brazhnik et al., 2008; Usunoff et al., 2009; Ibáñez-Sandoval et al., 2010; Tlamsa and Brumberg, 2010) and to our knowledge an examination across multiple topographic regions has not been…”

“, 2007) and prominent in the striatum (Wilson, 2007), play a critical role in coordinating activity during learning.”

“…striatum, there have been relatively few anatomical studies of the macrocircuitry of the mouse (White and DeAmicis, 1977; Hersch and White, 1982; Porter and White, 1983; Bernardo and Woolsey, 1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al., 2003; Miura et al., 2007;…”

“The importance of the amygdalostriatal projection into dorsal striatum was further suggested by the observation that it is an evolutionarily ancient pathway (Martínez-García et al., 2002) – present at least as far back as reptiles (Novejarque et al., 2004).”

“…been relatively few anatomical studies of the macrocircuitry of the mouse (White and DeAmicis, 1977; Hersch and White, 1982; Porter and White, 1983; Bernardo and Woolsey, 1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al., 2003; Miura et al., 2007; Brazhnik et al., 2008;…”

“Although it has received less attention as an important axis of functional differentiation, recent results suggest that the anterior and posterior striatum have dissociable behavioral effects (Tricomi et al., 2009; Shiflett et al., 2010).”

“This is also the case in the primate, but an elegant series of studies demonstrated a robust convergence of functionally related sensory and motor structures in the striatum despite this separation along the anterior–posterior axis (Ragsdale and Graybiel, 1990; Parthasarathy et al., 1992; Flaherty and Graybiel, 1995;…”

“For example, functional mapping studies (Brown, 1992; Brown and Sharp, 1995; Brown et al., 1996, 1998) and anatomical tracing experiments (Alloway et al.”

“In the rat sensory and motor projections to the striatum are only partially overlapping (Hoffer and Alloway, 2001; Alloway et al., 2006) even though sensory and motor areas at the same position in the anterior–posterior axis may converge more substantially (Ramanathan et al., 2002).”

“For example, functional mapping studies (Brown, 1992; Brown and Sharp, 1995; Brown et al., 1996, 1998) and anatomical tracing experiments (Alloway et al., 2000, 2006; Hoffer and Alloway, 2001; Ramanathan et al., 2002; Hoffer et al., 2005) have revealed that”

“…ProjectIon Although retrograde labeling of more lateral thalamic nuclei such as PO was previously observed in the rat (Erro et al., 2002; Alloway et al., 2006), we were nonetheless concerned that such labeling could result from leakage of some tracer in the neocortex during the…”

“For example, functional mapping studies (Brown, 1992; Brown and Sharp, 1995; Brown et al., 1996, 1998) and anatomical tracing experiments (Alloway et al., 2000, 2006; Hoffer and Alloway, 2001; Ramanathan et al., 2002; Hoffer et al., 2005) have revealed that”

“…on the vertebrate striatum, there have been relatively few anatomical studies of the macrocircuitry of the mouse (White and DeAmicis, 1977; Hersch and White, 1982; Porter and White, 1983; Bernardo and Woolsey, 1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al., 2003;…”

“…Porter and White, 1983; Bernardo and Woolsey, 1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al., 2003; Miura et al., 2007; Brazhnik et al., 2008; Usunoff et al., 2009; Ibáñez-Sandoval et al., 2010; Tlamsa and Brumberg, 2010) and to our knowledge an examination across…”

“However, while projections from the amygdala to the ventral striatum have indeed received quite a lot of attention (Gray, 1999; Cardinal et al., 2002; Floresco et al., 2008; Belin et al., 2009; Humphries and Prescott, 2010), the projections to the dorsal striatum that were observed with anterograde…”

“…of the mouse (White and DeAmicis, 1977; Hersch and White, 1982; Porter and White, 1983; Bernardo and Woolsey, 1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al., 2003; Miura et al., 2007; Brazhnik et al., 2008; Usunoff et al., 2009; Ibáñez-Sandoval et al., 2010;…”

“An important support for this model was a series of elegant studies in the monkey that revealed a convergence of functionally related, but anatomically distant, neocortical regions (Flaherty and Graybiel, 1991, 1995; Parthasarathy et al., 1992; Parthasarathy and Graybiel, 1997).”

“…1983; Bernardo and Woolsey, 1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al., 2003; Miura et al., 2007; Brazhnik et al., 2008; Usunoff et al., 2009; Ibáñez-Sandoval et al., 2010; Tlamsa and Brumberg, 2010) and to our knowledge an examination across multiple topographic…”

“Yet, despite the substantial literature on the vertebrate striatum, there have been relatively few anatomical studies of the macrocircuitry of the mouse (White and DeAmicis, 1977; Hersch and White, 1982; Porter and White, 1983; Bernardo and Woolsey, 1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al…”

“Our labeling was consistent with early studies in which injection of tritiated amino acids into the CEA and BLA revealed labeled axons across a large extent of the dorsal striatum in the rat (Kelley et al., 1982; Price, 1986).”

“…amygdalostriatal projection may be an important component of an extended learning circuit involving the hippocampus, dorsal striatum, and amygdala (McDonald et al., 2007). lIMItatIons of our dataset We selected fluorescent latex microspheres because of their lack of diffusion away from the…”

“…with sparse retrograde labeling we observed (Figure 4) and with the suggestion that only a subpopulation of neurons in lateral, posterior thalamic nuclei project to the striatum (Erro et al., 1999, 2001; BarrosoChinea et al., 2008). previously, were less commonly reported in the literature.”

“Brain Res. Rev. 58, 272–281. Tlamsa, A. P., and Brumberg, J. C. (2010). Organization and morphology of thalamocortical neurons of mouse ventral lateral thalamus. Somatosens. Mot. Res. 27, 34–43. Tricomi, E., Balleine, B. W., and O’Doherty, J. P. (2009). A specific role for posterior dorsolateral striatum in human habi…”

“…studies of the macrocircuitry of the mouse (White and DeAmicis, 1977; Hersch and White, 1982; Porter and White, 1983; Bernardo and Woolsey, 1987; Mattiace et al., 1989; Hofstetter and Ehret, 1992; Cepeda et al., 2003; Miura et al., 2007; Brazhnik et al., 2008; Usunoff et al., 2009;…”

“At 30 days post-injection (dpi), pSyn positive LB-like accumulations were exclusively ipsilateral to the injection site with the exception of the amygdala, to which the striatum projects bilaterally (23), suggesting that cell-to-cell transmission followed inter-neuronal connectivity.”

“…of rAAV2-retro extended to other circuits, specifically by characterizing the extent to which it labeled various afferents to the dorsomedial striatum (DMS), a part of the basal ganglia that receives long-range inputs from a variety of cortical and subcortical areas (Pan et al., 2010).”