Basal Ganglia and Cerebellar Inputs to ‘AIP’Dottie M. Clower1, Richard P. Dum1and Peter L. Strick1,2,31Pittsburgh Veterans Affairs Medical Center, University ofPittsburgh School of Medicine, Pittsburgh, PA, USA,2Centerfor the Neural Basis of Cognition, University of PittsburghSchool of Medicine, Pittsburgh, PA, USA and3Departmentsof Neurobiology, Neurosurgery and Psychiatry, Universityof Pittsburgh School of Medicine, Pittsburgh, PA, USAThe anterior intraparietal area (AIP) is a subregion of area 7b inposterior parietal cortex. AIP neurons respond to the sight of objects,as well as to the act of grasping them. We used retrograde trans-neuronal transport of rabies virus to examine subcortical inputs toAIP in the monkey. Virus transport labeled substantial numbers ofneurons in the substantia nigra pars reticulata (SNpr), as well as inthe dentate nucleus of the cerebellum. The hotspots of labeledneurons in SNpr and in dentate after AIP injections were separatefrom those created by virus injections into several other parietal orfrontal regions. These observations provide the first evidence thata major output nucleus of the basal ganglia, the SNpr, projects toa region of posterior parietal cortex. In addition, our findings providefurther support for the concept that posterior parietal cortex is atarget of cerebellar output.Keywords: basal ganglia, cerebellum, dentate nucleus, posterior parietalcortex, rabies virus, substantia nigra, transneuronal tracingIntroductionPhysiological and anatomical studies in monkeys have identifieda unique subregion of area 7b within inferior parietal cortextermed the anterior intraparietal area (AIP). AIP neurons eitherhave visual responses to the three-dimensional features ofobjects, motor responses to object manipulation or the combin-ation of the two types of responses (Godschalk and Lemon, 1989;Taira et al., 1990; Sakata and Taira, 1994; Sakata et al., 1995, 1998;Murata et al., 1996, 2000). AIP can be defined anatomically basedon its extensive interconnections with the ventral premotor area(PMv or area F5) (Chavis and Pandya, 1976; Petrides and Pandya,1984; Godschalk et al., 1984; Matelli et al., 1984, 1986; Neal et al.,1990; Ghosh and Gattera, 1995; Luppino et al., 1999; Tanne-Gariepy et al., 2002; see also Preuss and Goldman-Rakic, 1991;Lewis and Van Essen, 2000). Indeed, neurons in the PMv displayvisuomotor responses that are in many respects similar to thoseof AIP neurons. However, AIP contains more neurons that are ex-clusively responsive to the visual features of an object, whereasPMv contains more neurons that are selectively responsiveduring movement (Murata et al., 1997, 2000). Thus, AIP andPMv are thought to be nodes in a cortical network concernedwith processing the visual features of objects to specify theappropriate grasping patterns for manipulating them (Sakataet al., 1997; Oztop and Arbib, 2002).With the exception of some cortical interconnections, theanatomical inputs to AIP have not been well characterized. Inrecent studies we have shown that an adjacent portion of area 7is the target of output from the dentate nucleus of thecerebellum while other portions of area 7 receive input fromeither the superior colliculus or CA1 of the hippocampus(Clower et al., 2001a). We wondered whether one or all ofthese subcortical systems were a source of input to AIP. Forexample, perhaps some of the ‘visual’ properties of AIP neuronsare the result of input from the superior colliculus. Similarly,some of the ‘motor’ properties of AIP neurons could bea consequence of input from the cerebellum. In addition, giventhe extensive interconnections between AIP and PMv, wesought to examine whether these two cortical areas receivedinputs from common sources. PMv is the target of output fromboth the dentate and the internal segment of the globus pallidus(GPi) (Hoover and Strick, 1993; Dum and Strick, 2002). Whilethere is no prior evidence for basal ganglia input to regions ofposterior parietal cortex, some basal ganglia disorders result insymptoms that closely mimic parietal lobe dysfunction (Dantaand Hilton, 1975; Boller et al., 1984; Richards et al. , 1993;Hocherman and Giladi, 1998; Barrett et al., 2001; Lee et al.,2001a,b; Montse et al., 2001). These observations raise thepossibility that regions of posterior parietal cortex might also betargets of output from the basal ganglia.To examine these issues, we used retrograde transneuronaltransport of rabies virus after localized injections into AIP. Theparameters for using rabies as a transneuronal tracer have beenexamined extensively in the cebus monkey (e.g. Kelly andStrick, 2000, 2003). In addition, we have examined the sub-cortical inputs to a number of cortical regions in the cebusmonkey, including areas of posterior parietal, motor, prefrontaland inferotemporal cortex (Hoover and Strick, 1993, 1999;Lynch et al., 1994; Middleton and Strick, 1996, 1997, 2001;Clower et al., 2001a,b; Middleton and Strick, 2001; Dum andStrick, 2003). To be able to use all of this prior data forcomparison, we chose to perform this experiment in the samespecies. However, prior anatomical and physiological experi-ments on AIP have been performed in macaques. Because AIPcan be defined based on its interconnections with PMv, we usedthis anatomical feature to identify the location of AIP in thecebus monkey. We then injected the cebus AIP with rabies virusto define its subcortical inputs.Our results show that AIP is the target of both basal gangliaand cerebellar output. Approximately equivalent numbers ofneurons from each subcortical system project to AIP. Inaddition, the number of basal ganglia and cerebellar neuronsthat project to AIP is comparable to the number that project toindividual areas of premotor and prefrontal cortex. Further-more, the origins of the densest subcortical inputs to AIP arelargely separate from the origins of the densest input to PMv.Abstracts of some of these results have been reported else-where (Clower et al., 2001b, 2002).Materials and MethodsThe procedures adopted for this study and the care provided experi-mental animals conformed to the regulations detailed in the NationalCerebral Cortex V 15 N 7  Oxford University Press 2004; all rights reservedCerebral Cortex July 2005;15:913--920doi:10.1093/cercor/bhh190Advance Access publication September 30, 2004Institutes of Health Guide for the Care and Use of Laboratory Animals.All protocols were reviewed and approved by the Institutional