Abstract
The neural mechanisms involved in the selective processing of salient or behaviourally important stimuli are uncertain. We used an aversive conditioning paradigm in human volunteer subjects to manipulate the salience of visual stimuli (emotionally expressive faces) presented during positron emission tomography (PET) neuroimaging. Increases in salience, and conflicts between the innate and acquired value of the stimuli, produced augmented activation of the pulvinar nucleus of the right thalamus. Furthermore, this pulvinar activity correlated positively with responses in structures hypothesized to mediate value in the brain right amygdala and basal forebrain (including the cholinergic nucleus basalis of Meynert). The results provide evidence that the pulvinar nucleus of the thalamus plays a crucial modulatory role in selective visual processing, and that changes in perceptual salience are mediated by value-dependent plasticity in pulvinar responses.
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- Acquas E., Wilson C., Fibiger H. C. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation, and fear. J Neurosci. 1996 May 1;16(9):3089–3096. doi: 10.1523/JNEUROSCI.16-09-03089.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Adolphs R., Tranel D., Damasio H., Damasio A. R. Fear and the human amygdala. J Neurosci. 1995 Sep;15(9):5879–5891. doi: 10.1523/JNEUROSCI.15-09-05879.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bechara A., Tranel D., Damasio H., Adolphs R., Rockland C., Damasio A. R. Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science. 1995 Aug 25;269(5227):1115–1118. doi: 10.1126/science.7652558. [DOI] [PubMed] [Google Scholar]
- Bowers D., Bauer R. M., Coslett H. B., Heilman K. M. Processing of faces by patients with unilateral hemisphere lesions. I. Dissociation between judgments of facial affect and facial identity. Brain Cogn. 1985 Jul;4(3):258–272. doi: 10.1016/0278-2626(85)90020-x. [DOI] [PubMed] [Google Scholar]
- Bushnell M. C., Goldberg M. E., Robinson D. L. Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention. J Neurophysiol. 1981 Oct;46(4):755–772. doi: 10.1152/jn.1981.46.4.755. [DOI] [PubMed] [Google Scholar]
- Campeau S., Davis M. Involvement of the central nucleus and basolateral complex of the amygdala in fear conditioning measured with fear-potentiated startle in rats trained concurrently with auditory and visual conditioned stimuli. J Neurosci. 1995 Mar;15(3 Pt 2):2301–2311. doi: 10.1523/JNEUROSCI.15-03-02301.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeKosky S. T., Heilman K. M., Bowers D., Valenstein E. Recognition and discrimination of emotional faces and pictures. Brain Lang. 1980 Mar;9(2):206–214. doi: 10.1016/0093-934x(80)90141-8. [DOI] [PubMed] [Google Scholar]
- Field T. M., Woodson R., Greenberg R., Cohen D. Discrimination and imitation of facial expression by neonates. Science. 1982 Oct 8;218(4568):179–181. doi: 10.1126/science.7123230. [DOI] [PubMed] [Google Scholar]
- Friston K. J., Tononi G., Reeke G. N., Jr, Sporns O., Edelman G. M. Value-dependent selection in the brain: simulation in a synthetic neural model. Neuroscience. 1994 Mar;59(2):229–243. doi: 10.1016/0306-4522(94)90592-4. [DOI] [PubMed] [Google Scholar]
- Hamm A. O., Greenwald M. K., Bradley M. M., Lang P. J. Emotional learning, hedonic change, and the startle probe. J Abnorm Psychol. 1993 Aug;102(3):453–465. doi: 10.1037//0021-843x.102.3.453. [DOI] [PubMed] [Google Scholar]
- Hars B., Maho C., Edeline J. M., Hennevin E. Basal forebrain stimulation facilitates tone-evoked responses in the auditory cortex of awake rat. Neuroscience. 1993 Sep;56(1):61–74. doi: 10.1016/0306-4522(93)90562-t. [DOI] [PubMed] [Google Scholar]
- Hawkins R. D., Abrams T. W., Carew T. J., Kandel E. R. A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science. 1983 Jan 28;219(4583):400–405. doi: 10.1126/science.6294833. [DOI] [PubMed] [Google Scholar]
- Hodes R. L., Cook E. W., 3rd, Lang P. J. Individual differences in autonomic response: conditioned association or conditioned fear? Psychophysiology. 1985 Sep;22(5):545–560. doi: 10.1111/j.1469-8986.1985.tb01649.x. [DOI] [PubMed] [Google Scholar]
- Hugdahl K., Berardi A., Thompson W. L., Kosslyn S. M., Macy R., Baker D. P., Alpert N. M., LeDoux J. E. Brain mechanisms in human classical conditioning: a PET blood flow study. Neuroreport. 1995 Sep 11;6(13):1723–1728. doi: 10.1097/00001756-199509000-00005. [DOI] [PubMed] [Google Scholar]
- Johnsen B. H., Hugdahl K. Right hemisphere representation of autonomic conditioning to facial emotional expressions. Psychophysiology. 1993 May;30(3):274–278. doi: 10.1111/j.1469-8986.1993.tb03353.x. [DOI] [PubMed] [Google Scholar]
- Jones B., Mishkin M. Limbic lesions and the problem of stimulus--reinforcement associations. Exp Neurol. 1972 Aug;36(2):362–377. doi: 10.1016/0014-4886(72)90030-1. [DOI] [PubMed] [Google Scholar]
- Kandel E. R., Schwartz J. H. Molecular biology of learning: modulation of transmitter release. Science. 1982 Oct 29;218(4571):433–443. doi: 10.1126/science.6289442. [DOI] [PubMed] [Google Scholar]
- LaBar K. S., LeDoux J. E., Spencer D. D., Phelps E. A. Impaired fear conditioning following unilateral temporal lobectomy in humans. J Neurosci. 1995 Oct;15(10):6846–6855. doi: 10.1523/JNEUROSCI.15-10-06846.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LaBerge D., Buchsbaum M. S. Positron emission tomographic measurements of pulvinar activity during an attention task. J Neurosci. 1990 Feb;10(2):613–619. doi: 10.1523/JNEUROSCI.10-02-00613.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lanzetta J. T., Orr S. P. Excitatory strength of expressive faces: effects of happy and fear expressions and context on the extinction of a conditioned fear response. J Pers Soc Psychol. 1986 Jan;50(1):190–194. doi: 10.1037//0022-3514.50.1.190. [DOI] [PubMed] [Google Scholar]
- LeDoux J. E. Emotional memory systems in the brain. Behav Brain Res. 1993 Dec 20;58(1-2):69–79. doi: 10.1016/0166-4328(93)90091-4. [DOI] [PubMed] [Google Scholar]
- LeDoux J. E., Iwata J., Cicchetti P., Reis D. J. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J Neurosci. 1988 Jul;8(7):2517–2529. doi: 10.1523/JNEUROSCI.08-07-02517.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LeDoux J. E., Sakaguchi A., Reis D. J. Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli. J Neurosci. 1984 Mar;4(3):683–698. doi: 10.1523/JNEUROSCI.04-03-00683.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Moran J., Desimone R. Selective attention gates visual processing in the extrastriate cortex. Science. 1985 Aug 23;229(4715):782–784. doi: 10.1126/science.4023713. [DOI] [PubMed] [Google Scholar]
- Morgan M. A., Romanski L. M., LeDoux J. E. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Lett. 1993 Nov 26;163(1):109–113. doi: 10.1016/0304-3940(93)90241-c. [DOI] [PubMed] [Google Scholar]
- Morris J. S., Frith C. D., Perrett D. I., Rowland D., Young A. W., Calder A. J., Dolan R. J. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature. 1996 Oct 31;383(6603):812–815. doi: 10.1038/383812a0. [DOI] [PubMed] [Google Scholar]
- Ohman A., Dimberg U. Facial expressions as conditioned stimuli for electrodermal responses: a case of "preparedness"? J Pers Soc Psychol. 1978 Nov;36(11):1251–1258. doi: 10.1037//0022-3514.36.11.1251. [DOI] [PubMed] [Google Scholar]
- Olshausen B. A., Anderson C. H., Van Essen D. C. A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information. J Neurosci. 1993 Nov;13(11):4700–4719. doi: 10.1523/JNEUROSCI.13-11-04700.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Petersen S. E., Robinson D. L., Morris J. D. Contributions of the pulvinar to visual spatial attention. Neuropsychologia. 1987;25(1A):97–105. doi: 10.1016/0028-3932(87)90046-7. [DOI] [PubMed] [Google Scholar]
- Pirch J. H., Turco K., Rucker H. K. A role for acetylcholine in conditioning-related responses of rat frontal cortex neurons: microiontophoretic evidence. Brain Res. 1992 Jul 17;586(1):19–26. doi: 10.1016/0006-8993(92)91366-m. [DOI] [PubMed] [Google Scholar]
- Rafal R. D., Posner M. I. Deficits in human visual spatial attention following thalamic lesions. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7349–7353. doi: 10.1073/pnas.84.20.7349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rapcsak S. Z., Kaszniak A. W., Rubens A. B. Anomia for facial expressions: evidence for a category specific visual-verbal disconnection syndrome. Neuropsychologia. 1989;27(8):1031–1041. doi: 10.1016/0028-3932(89)90183-8. [DOI] [PubMed] [Google Scholar]
- Roberts A. C., Robbins T. W., Everitt B. J., Muir J. L. A specific form of cognitive rigidity following excitotoxic lesions of the basal forebrain in marmosets. Neuroscience. 1992;47(2):251–264. doi: 10.1016/0306-4522(92)90241-s. [DOI] [PubMed] [Google Scholar]
- Robinson D. L., Petersen S. E. The pulvinar and visual salience. Trends Neurosci. 1992 Apr;15(4):127–132. doi: 10.1016/0166-2236(92)90354-b. [DOI] [PubMed] [Google Scholar]
- Russchen F. T., Amaral D. G., Price J. L. The afferent connections of the substantia innominata in the monkey, Macaca fascicularis. J Comp Neurol. 1985 Dec 1;242(1):1–27. doi: 10.1002/cne.902420102. [DOI] [PubMed] [Google Scholar]
- Russchen F. T., Bakst I., Amaral D. G., Price J. L. The amygdalostriatal projections in the monkey. An anterograde tracing study. Brain Res. 1985 Mar 11;329(1-2):241–257. doi: 10.1016/0006-8993(85)90530-x. [DOI] [PubMed] [Google Scholar]
- Thorpe S. J., Rolls E. T., Maddison S. The orbitofrontal cortex: neuronal activity in the behaving monkey. Exp Brain Res. 1983;49(1):93–115. doi: 10.1007/BF00235545. [DOI] [PubMed] [Google Scholar]
- Ungerleider L. G., Galkin T. W., Mishkin M. Visuotopic organization of projections from striate cortex to inferior and lateral pulvinar in rhesus monkey. J Comp Neurol. 1983 Jun 20;217(2):137–157. doi: 10.1002/cne.902170203. [DOI] [PubMed] [Google Scholar]
- WEISKRANTZ L. Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J Comp Physiol Psychol. 1956 Aug;49(4):381–391. doi: 10.1037/h0088009. [DOI] [PubMed] [Google Scholar]
- Wilson F. A., Rolls E. T. Neuronal responses related to reinforcement in the primate basal forebrain. Brain Res. 1990 Feb 19;509(2):213–231. doi: 10.1016/0006-8993(90)90546-n. [DOI] [PubMed] [Google Scholar]