Destruction and creation of spatial tuning by disinhibition: GABA(A) blockade of prefrontal cortical neurons engaged by working memory

Journal of Neuroscience

Volumn 20, Issue 1, 2000, Pages 485-494

  Rao, Srinivas G ^a   Williams, Graham V ^a   Goldman Rakic, Patricia S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bicuculline; Fast spiking; Inhibition; Interneurons; Prefrontal cortex; Primate; Spatial tuning; Working memory

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

ARTICLE; CONTROLLED STUDY; INTERNEURON; IONTOPHORESIS; MACACA; NEUROMODULATION; NONHUMAN; PHARMACOLOGICAL BLOCKING; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RECEPTOR BLOCKING; WORKING MEMORY;

EID: 0033995269     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-01-00485.2000     Document Type: Article

References (44)

1. Alloway KD, Burton H (1991) Differential effects of GABA and bicuculline on rapidly- and slowly-adapting neurons in primary somatosensory cortex of primates. Exp Brain Res 85:598-610.
2. Alloway KD, Rosenthal P, Burton H (1989) Quantitative measurements of receptive field changes during antagonism of GABAergic transmission in primary somatosensory cortex of eats. Exp Brain Res 78:514-532.
3. Baddeley A (1992) Working memory. Science 255:556-559.
4. Chafee MV, Goldman-Rakic PS (1998) Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. J Neurophysiol 79:2919-2940.
5. Douglas RJ, Koch C, Mahowald M, Martin KAC, Suarez HH (1995) Recurrent excitation in neocortical circuits. Science 269:981-985.
6. Eysel UT, Crook JM, Machemer HF (1990) GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex. Exp Brain Res 80:626-630.
7. Eysel UT, Shevelev IA, Lazareva NA, Sharaev GA (1998) Orientation tuning and receptive field structure in cat striate neurons during local blockade of intracortical inhibition. Neuroscience 84:25-36.
8. Fisher NI (1993) Statistical analysis of circular data. Cambridge: Cambridge UP.
9. Funahashi S, Bruce CJ, Goldman-Rakic PS (1989) Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61:331-349.
10. Funahashi S, Bruce CJ, Goldman-Rakic PS (1990) Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. J Neurophysiol 63:814-831.
11. Funahashi S, Bruce CJ, Goldman-Rakic PS (1991) Neuronal activity related to saccadic eye movements in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 65:1464-1483.
12. Gabbott PL, Bacon SJ (1996) Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: I. Cell morphology and morphometrics. J Comp Neurol 364:567-608.
13. Goldman PS, Nauta WJ (1977) Columnar distribution of cortico-cortical fibers in the frontal association, limbic, and motor cortex of the developing rhesus monkey. Brain Res 122:393-413.
14. Goldman-Rakic PS (1987) Circuitry of the frontal association cortex and its relevance to dementia. Arch Gerontol Geriat 6:299-309.
15. Goldman-Rakic PS (1995a) Architecture of the prefrontal cortex and the central executive. Ann NY Acad Sci 769:71-83.
16. Goldman-Rakic PS (1995b) Cellular basis of working memory. Neuron 14:477-485.
17. Gonchar Y, Burkhalter A (1999) Differential subcellular localization of forward and feedback interareal inputs to parvalbumin expressing GABAergic neurons in rat visual cortex. J Comp Neurol 406:346-360.
18. Jacobs KM, Donoghue JP (1991) Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251:944-947.
19. Jones EG (1993) GABAergic neurons and their role in cortical plasticity in primates. Cereb Cortex 3:361-372.
20. Kawaguchi Y (1993) Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69:416-431.
21. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638-2655.
22. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486.
23. Kisvarday ZF, Beaulieu C, Eysel UT (1993) Network of GABAergic large basket cells in cat visual cortex (area 18): implication for lateral disinhibition. J Comp Neurol 327:398-415.
24. Kyriazi HT, Carvell GE, Brumberg JC, Simons DJ (1996) Quantitative effects of GABA and bicuculline methiodide on receptive field properties of neurons in real and simulated whisker barrels. J Neurophysiol 75:547-560.
25. Lisman JE, Fallon JR (1999) What maintains memories? Science 283:339-340.
26. Lisman JE, Fellous JM, Wang XJ (1998) A role for NMDA-receptor channels in working memory. Nat Neurosci 1:273-275.
27. Murthy A, Humphrey AL (1999) Inhibitory contributions to spatiotemporal receptive-field structure and direction selectivity in simple cells of cat area 17. J Neurophysiol 81:1212-1224.
28. Rao SG, Williams GV, Goldman-Rakic PS (1999) Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. J Neurophysiol 81:1903-1916.
29. Sato H, Katsuyama N, Tamura H, Hata Y, Tsumoto T (1996) Mechanisms underlying orientation selectivity of neurons in the primary visual cortex of the macaque. J Physiol (Lond) 494:757-771.
30. Sawaguchi T, Goldman-Rakic PS (1994) The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. J Neurophysiol 71:515-528.
31. Sawaguchi T, Matsumura M, Kubota K (1988) Delayed response deficit in monkeys by locally disturbed prefrontal neuronal activity by bicuculline. Behav Brain Res 31:193-198.
32. Sawaguchi T, Matsumura M, Kubota K (1989) Delayed response deficits produced by local injection of bicuculline into the dorsolateral prefrontal cortex in Japanese macaque monkeys. Exp Brain Res 75:457-469.
33. Sillito AM (1984) Functional considerations of the operation of GABAergic inhibitory processes in the visual cortex. In: Cerebral cortex, Ed 2 (Jones EG, Peters A, eds), pp 91-117. New York: Plenum.
34. Tamas G, Buhl EH, Somogyi P (1997) Massive autaptic self-innervation of GABAergic neurons in cat visual cortex. J Neurosci 17:6352-6364.
35. Tamas G, Somogyi P, Buhl EH (1998) Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat. J Neurosci 18:4255-4270.
36. Thomson AM, Deuchars J (1997) Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb Cortex 7:510-522.
37. Thomson AM, West DC, Hahn J, Deuchars J (1996) Single axon IPSPs elicited in pyramidal cells by three classes of interneurones in slices of rat neocortex. J Physiol (Lond) 496:81-102.
38. - conductance in cultured rat hippocampal neurones. J Physiol (Lond) 479:53-63.
39. Williams GV, Rao SG, Goldman-Rakic PS (1997) Attenuation of memory fields in primate prefrontal cortical pyramidal cells and interneurons by selective 5-HT2 antagonists. Soc Neurosci Abstr 23:627.7.
40. Williams GV, Rao SG, Goldman-Rakic PS (1998a) Serotonin2 receptor modulation of mnemonic coding in prefrontal cortex. Biol Psychiatry 43:7S.
41. Williams GV, Rao SG, Leung H-C, Goldman-Rakic PS (1998b) Effects of dopamine D4 antagonists on mnemonic activity of neurons in primate prefrontal cortex. Biol Psychiatry 43:41-42S.
42. Williams SM, Goldman-Rakic PS, Leranth C (1992) The synaptology of parvalbumin-immunoreactive neurons in the primate prefrontal cortex. J Comp Neurol 320:353-369.
43. Wilson FS, O'Scalaidhe SP, Goldman-Rakic PS (1994) Functional synergism between putative gamma-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. Proc Natl Acad Sci USA 91:4009-4013.
44. Xi ZX, Akasu T (1996) Presynaptic GABAA receptors in vertebrate synapses. Kurume Med J 43:115-122.