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Left and right basal ganglia and frontal activity during language generation: Contributions to lexical, semantic, and phonological processes

Published online by Cambridge University Press:  12 February 2004

BRUCE CROSSON ,
HOPE BENEFIELD ,
M. ALLISON CATO ,
JOSEPH R. SADEK ,
ANNA BACON MOORE ,
CHRISTINA E. WIERENGA ,
KAUNDINYA GOPINATH ,
DAVID SOLTYSIK ,
RUSSELL M. BAUER  and
EDWARD J. AUERBACH
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BRUCE CROSSON
Affiliation:
McKnight Brain Institute, University of Florida, Gainsville Department of Clinical and Health Psychology, University of Florida, Gainsville Veterans Affairs Brain Rehabilitation Research Center, Gainsville, Florida
HOPE BENEFIELD
Affiliation:
McKnight Brain Institute, University of Florida, Gainsville Department of Clinical and Health Psychology, University of Florida, Gainsville
M. ALLISON CATO
Affiliation:
McKnight Brain Institute, University of Florida, Gainsville Department of Clinical and Health Psychology, University of Florida, Gainsville
JOSEPH R. SADEK
Affiliation:
Department of Psychiatry, University of California, San Diego
ANNA BACON MOORE
Affiliation:
McKnight Brain Institute, University of Florida, Gainsville Department of Clinical and Health Psychology, University of Florida, Gainsville Veterans Affairs Brain Rehabilitation Research Center, Gainsville, Florida
CHRISTINA E. WIERENGA
Affiliation:
McKnight Brain Institute, University of Florida, Gainsville Department of Clinical and Health Psychology, University of Florida, Gainsville
KAUNDINYA GOPINATH
Affiliation:
McKnight Brain Institute, University of Florida, Gainsville Department of Radiology, University of Florida, Gainsville
DAVID SOLTYSIK
Affiliation:
McKnight Brain Institute, University of Florida, Gainsville Department of Radiology, University of Florida, Gainsville
RUSSELL M. BAUER
Affiliation:
McKnight Brain Institute, University of Florida, Gainsville Department of Clinical and Health Psychology, University of Florida, Gainsville
EDWARD J. AUERBACH
Affiliation:
University of Minnesota Center for Magnetic Resonance Research, Department of Radiology, Minneapolis
DIDEM GÖKÇAY
Affiliation:
Institute for Neural Computation, University of California, San Diego
CHRISTIANA M. LEONARD
Affiliation:
McKnight Brain Institute, University of Florida, Gainsville Department of Neuroscience, University of Florida, Gainsville
RICHARD W. BRIGGS
Affiliation:
McKnight Brain Institute, University of Florida, Gainsville Department of Radiology, University of Florida, Gainsville
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Abstract

fMRI was used to determine the frontal, basal ganglia, and thalamic structures engaged by three facets of language generation: lexical status of generated items, the use of semantic vs. phonological information during language generation, and rate of generation. During fMRI, 21 neurologically normal subjects performed four tasks: generation of nonsense syllables given beginning and ending consonant blends, generation of words given a rhyming word, generation of words given a semantic category at a fast rate (matched to the rate of nonsense syllable generation), and generation of words given a semantic category at a slow rate (matched to the rate of generating of rhyming words). Components of a left pre-SMA–dorsal caudate nucleus–ventral anterior thalamic loop were active during word generation from rhyming or category cues but not during nonsense syllable generation. Findings indicate that this loop is involved in retrieving words from pre-existing lexical stores. Relatively diffuse activity in the right basal ganglia (caudate nucleus and putamen) also was found during word-generation tasks but not during nonsense syllable generation. Given the relative absence of right frontal activity during the word generation tasks, we suggest that the right basal ganglia activity serves to suppress right frontal activity, preventing right frontal structures from interfering with language production. Current findings establish roles for the left and the right basal ganglia in word generation. Hypotheses are discussed for future research to help refine our understanding of basal ganglia functions in language generation. (JINS, 2003, 9, 1061–1077.)

Keywords

Basal gangliafMRILanguageThalamus
Type
THEMATIC ARTICLES
Information
Journal of the International Neuropsychological Society , Volume 9 , Issue 7 , November 2003 , pp. 1061 - 1077
Copyright
© 2003 The International Neuropsychological Society

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References

REFERENCES

Akkal, D., Dum, R.P., & Strick, P.L. (2002). Cerebellar and basal ganglia inputs to the pre-supplementary area (Pre-SMA). Society for Neuroscience Abstract Viewer/Itinerary Planner, Online, Program No. 462. 14.
Bandettini, P.A., Jesmanowicz, A., Wong, E.C., & Hyde, J.S. (1993). Processing strategies for time-course data sets in functional MRI of the human brain. Magnetic Resonance in Medicine, 30, 161–173.Google Scholar
Barch, D.M., Braver, T.S., Saab, F.W., & Noll, D.C. (2000). Anterior cingulate and the monitoring of response conflict: Evidence from an fMRI study of overt verb generation. Journal of Cognitive Neuroscience, 12, 298–309.Google Scholar
Botvinick, M., Nystrom, L.E., Fissell, K., Carter, C.S., & Cohen, J.D. (1999). Conflict monitoring versus selection for action in anterior cingulate cortex. Nature, 402, 179–181.Google Scholar
Broadbent, G. (1872). On the cerebral mechanisms of speech and thought. London.
Buchanan, S.L., Thompson, R.H., Maxwell, B.L., & Powell, D.A. (1994). Efferent connections of the medial prefrontal cortex in the rabbit. Experimental Brain Research, 100, 469–483.Google Scholar
Bullmore, E., Brammer, M., Williams, S.C.R., Rabe-Hesketh, S., Janot, N., David, A., Mellers, J., Howard, R., & Sham, P. (1996). Statistical methods of estimation and inference for functional MR image analysis. Magnetic Resonance in Medicine, 35, 261–277.Google Scholar
Cabeza, R. & Nyberg, L. (2000). Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience, 12, 1–47.Google Scholar
Carter, C.S., Macdonald, A.M., Botvinick, M., Ross, L.L., Stenger, A., Noll, D., & Cohen, J.D. (2000). Parsing executive processes: Strategic vs. evaluative functions of the anterior cingulate cortex. Proceedings of the National Academy of Sciences, U.S.A., 97, 1944–1948.Google Scholar
Chao, L.L., Haxby, J.V., & Martin, A. (1999). Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects. Nature Neuroscience, 2, 913–919.Google Scholar
Copland, D.A., Chenery, H.J., & Murdoch, B.E. (2000a). Processing lexical ambiguities in word triplets: Evidence of lexical–semantic deficits following dominant nonthalamic subcortical lesions. Neuropsychology, 14, 379–390.Google Scholar
Copland, D.A., Chenery, H.J., & Murdoch, B.E. (2000b). Persistent deficits in complex language function following dominant nonthalamic subcortical lesions. Journal of Medical Speech-Language Pathology, 8, 1–15.Google Scholar
Cowan, R.L. & Wilson, C.J. (1994). Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. Journal of Neurophysiology, 71, 17–32.Google Scholar
Cox, R.W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance images. Computers in Biomedical Research, 29, 162–173.Google Scholar
Crosson, B., Sadek, J.R., Maron, L., Gökçay, D., Mohr, C.M., Auerbach, E.J., Freeman, A.J., Leonard, C.M., Briggs, R.W. (2001). Relative shift in activity from medial to lateral frontal cortex during internally versus externally guided word generation. Journal of Cognitive Neuroscience, 13, 272–283.Google Scholar
Crosson, B., Sadek, J.R., Bobholz, J.A., Gökçay, D., Mohr, C.M., Leonard, C.M., Maron, L., Auerbach, E.J., Browd, S.R., Freeman, A.J., & Briggs, R.W. (1999). Activity in the paracingulate and cingulate sulci during word generation: An fMRI study of functional anatomy. Cerebral Cortex, 9, 307–316.Google Scholar
Crosson, B., Williamson, D.J.G., Shukla, S.S., Honeyman, J.C., & Nadeau, S.E. (1994). A technique for localizing activation in the human brain with [99mTc]-HMPAO SPECT: A validation study using visual stimulation. Journal of Nuclear Medicine, 35, 755–763.Google Scholar
Forman, S.D., Cohen, J.D., Fitzgerald, M., Eddy, W.F., Mintun, M.A., & Noll, D.C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magnetic Resonance in Medicine, 33, 636–647.Google Scholar
Gerfen, C.R. (1992). The neostriatal mosaic: Multiple levels of compartmental organization in the basal ganglia. Annual Review of Neuroscience, 15, 285–320.Google Scholar
Heilman, K.M., Watson, R.T., & Valenstein, E. (2003). Neglect and related disorders. In K.M. Heilman & E. Valenstein (Eds.), Clinical neuropsychology (4th ed., pp. 296–346). New York: Oxford University Press.
Hoover, J.E. & Strick, P.L. (1999). The organization of cerebellar and basal ganglia outputs to primary motor cortex as revealed by retrograde transneuronal transport of herpes simplex virus type 1. Journal of Neuroscience, 19, 1446–1463.Google Scholar
Inase, M., Tokuno, H., Nambu, A., Akazawa, T., & Takada, M. (1999). Corticostriatal and corticosubthalamic input zones from the presupplementary motor area in the macaque monkey: Comparison with the input zones from the supplementary motor area. Brain Research, 833, 191–201.Google Scholar
Jueptner, M. & Weiller, C. (1998). A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. Brain, 121, 1437–1449.Google Scholar
King, K.F., Foo, T.K.F., & Crawford, C.R. (1995). Optimized gradient waveforms for spiral scanning. Magnnetic Resonance in Medicine, 34, 156–160.Google Scholar
Lauritzen, M. (2001). Relationship of spikes, synaptic activity, and local changes of cerebral blood flow. Journal of Cerebral Blood Flow and Metabolism, 21, 1367–1383.Google Scholar
Macovski, A. (1985). Volumetric NMR imaging with time-varying gradients. Magnetic Resonance in Medicine, 2, 29–40.Google Scholar
Marie, P. (1906). Revision de la question de l'aphasie: Que faut-il penser des aphasies sous-corticales (aphasies pures)? [Review of the question of aphasia: What to think about subcortical aphasias (pure aphasias)?] La Semaine Medicale, 42.Google Scholar
Matsuzaka, Y., Aizawa, H., Tanji, J. (1992). A motor area rostral to the supplementary motor area (presupplementary motor area) in the monkey: Neuronal activity during a learned motor task. Journal of Neurophysiology, 68, 653–662.Google Scholar
Mega, M.S. & Alexander, M.P. (1994). Subcortical aphasia: The core profile of capsulostriatal infarction. Neurology, 44, 1824–1829.Google Scholar
Middleton, F.A. & Strick, P.L. (2000). Basal ganglia and cerebellar loops: Motor and cognitive circuits. Brain Research Review, 31, 236–250.Google Scholar
Milham, M.P., Banich, M.T., Webb, A., Barad, V., Cohen, N.J., Wszalek, T., & Kramer, A.F. (2001). The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of conflict. Brain Research: Cognitive Brain Research, 12, 467–473.Google Scholar
Mink, J.W. (1996). The basal ganglia: Focused selection and inhibition of competing motor programs. Progress in Neurobiology, 50, 381–425.Google Scholar
Morino, P., Mascangni, F., McDonald, A., & Hökfelt, T. (1994). Cholecystokinin corticostriatal pathway in the rat: Evidence for bilateral origin from medial prefrontal cortical areas. Neuroscience, 59, 939–952.Google Scholar
Nadeau, S.E. & Crosson, B. (1997). Subcortical aphasia. Brain and Language, 58, 355–402.Google Scholar
Nadeau, S.E., Hammond, E., Williamson, D.J., & Crosson, B. (1997). Resting and stimulated states in functional imaging studies: Evidence of differences in attentional and intentional set. Neuropsychiatry, Neuropsychology, and Behavioral Neurology, 10, 162–163.Google Scholar
Nambu, A., Tokuna, H., Hamada, I., Kita, H., Imanishi, M., Akazawa, T., Ikeuchi, Y., & Hasegawa, N. (2000). Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. Journal of Neurophysiology, 84, 289–300.Google Scholar
Newman, S.D., Twieg, D.B., & Carpenter, P.A. (2001). Baseline conditions and subtractive logic in neuroimaging. Human Brain Mapping, 14, 228–235.Google Scholar
Noll, D.C., Cohen, J.D., Meyer, C.H., & Schneider, W.J. (1995). Spiral k-space MR imaging of cortical activation. Magnetic Resonance Imaging, 5, 49–56.Google Scholar
Ojemann, G.A. (1983). Brain organization for language from the perspective of electrical stimulation mapping. Behavioral and Brain Sciences, 2, 189–230.Google Scholar
Ojemann, J.G., Buckner, R.L., Akbudak, E., Snyder, A.Z., Ollinger, J.M., McKinstry, R.C., Rosen, B.R., Petersen, S.E., Raichle, M.E., & Conturo, T.E. (1998). Functional MRI studies of word-stem completion: Reliability across laboratories and comparison to blood flow imaging with PET. Human Brain Mapping, 6, 203–215.Google Scholar
Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsychologia, 9, 97–113.Google Scholar
Palmer, E.D., Rosen, H.J., Ojemann, J.G., Buckner, R.L., Kelley, W.M., & Petersen, S.E. (2001). An event-related fMRI study of overt and covert word stem completion. NeuroImage, 14, 182–193.Google Scholar
Parent, A. (1990). Extrinsic connections of the basal ganglia. Trends in Neuroscience, 13, 254–258.Google Scholar
Parent, A. & Hazrati, L.-N. (1993). Anatomical aspects of information processing in primate basal ganglia. Trends in Neuroscience, 16, 111–116.Google Scholar
Paus, T. (2001). Primate anterior cingulate cortex: Where motor control, drive and cognition interface. Nature Reviews Neuroscience, 2, 417–424.Google Scholar
Paus, T., Tomaiuolo, F., Otaky, N., MacDonald, D., Petrides, M., Atlas, J., Morris, R., & Evans, A.C. (1996). Human cingulate and paracingulate sulci: Pattern, variability, asymmetry, and probabilistic map. Cerebral Cortex, 6, 207–214.Google Scholar
Penney, J.B. & Young, A.B. (1986). Striatal inhomogeneities and basal ganglia function. Movement Disorders, 1, 3–15.Google Scholar
Petersen, S.E., Fox, P.T., Posner, M.I., Mintun, M., & Raichle, M.E. (1988). Positron emission tomographic studies of the cortical anatomy of single-word processing. Nature, 331, 585–589.Google Scholar
Picard, N. & Strick, P.L. (1996). Motor areas of the medial wall: A review of their location and functional activation. Cerebral Cortex, 6, 342–353.Google Scholar
Picard, N. & Strick, P.L. (2001). Imaging the premotor areas. Current Opinion in Neurobiology, 11, 263–272.Google Scholar
Redgrave, P., Prescott, T.J., & Gurney, K. (1999). The basal ganglia: A vertebrate solution to the selection problem? Neuroscience, 89, 1009–1023.Google Scholar
Rosen, H.J., Ojemann, J.G., Ollinger, J.M., & Petersen, S.E. (2000). Comparison of brain activation during word retrieval done silently and aloud using fMRI. Brain and Cognition, 42, 201–217.Google Scholar
Strick, P.L., Dum, R.P, & Picard, N. (1995). Macro-organization of the circuits connecting the basal ganglia with the cortical motor areas. In J.C. Houk, J.L. Davis, & D.G. Beiser (Eds.), Models of information processing in the basal ganglia (pp. 117–130). Cambridge, MA: MIT Press.
Talaraich, J. & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain. 3-dimensional proportional system: An Approach to cerebral imaging. New York: Thieme Medical Publishers.
van Veen, V., Cohen, J.D., Botvinick, M.M., Stenger, V.A., & Carter, C.S. (2001). Anterior cingulate cortex, conflict monitoring, and levels of processing. NeuroImage, 14, 1302–1308.Google Scholar
Wang, H. & Pickel, V.M. (1998). Dendritic spines containing μ-opioid receptors in rat striatal patches receive asymmetric synapses from prefrontal corticostriatal afferents. Journal of Comparative Neurology, 396, 223–237.Google Scholar
Warburton, E., Wise, R.J.S., Price, C.J., Weiller, C., Hadar, U., Ramsay, S., & Frackowiak, R.J.S. (1996). Noun and verb retrieval by normal subjects: Studies with PET. Brain, 119, 159–179.CrossRefGoogle Scholar
Weiller, C., Willmes, K., Reiche, W., Thron, A., Insensee, C., Buell, U., & Ringelstein, E.B. (1993). The case of aphasia or neglect after striatocapsular infarction. Brain, 116, 1509–1525.CrossRefGoogle Scholar
Wernicke, C. (1874). Der aphasische symptomencomplex [The complex of symptoms in aphasia]. Breslau, Germany: Cohn and Weigert.
Wiesendanger, R. & Wiesendanger, M. (1985). Thalamic connections with medial area 6 (supplementary motor cortex) in the monkey (Macaca fascicularis). Experimental Brain Research, 59, 91–104.Google Scholar