Abstract
OBJECTIVE—To investigate whether frontal lobe damage in humans disrupts the natural tendency to preferentially attend to novel visual events in the environment. METHODS—Nine patients with chronic infarctions in the dorsolateral prefrontal cortex (DLPFC) and 23 matched normal controls participated in a study in which subjects viewed repetitive background stimuli, infrequent target stimuli, and novel visual stimuli (for example, fragmented or "impossible" objects). Subjects controlled viewing duration by a button press that led to the onset of the next stimulus. They also responded to targets by pressing a foot pedal. The amount of time spent looking at the different kinds of stimuli, and the target detection accuracy and speed served as dependent variables. RESULTS—Overall, normal controls spent significantly more time than frontal lobe patients looking at novel stimuli. Analysis of responses across blocks showed that initially frontal lobe patients behaved like normal controls by directing more attention to novel than background stimuli. However, they quickly began to distribute their viewing time evenly between novel and background stimuli, a pattern that was strikingly different from normal controls. By contrast, there were no differences between frontal lobe patients and normal controls for viewing duration devoted to background and target stimuli, target detection accuracy, or reaction time to targets. Frontal lobe patients did not differ from normal controls in terms of age, education, estimated IQ, or mood, but were more apathetic as measured by self report and informants' judgments. Attenuated responses to novel stimuli significantly correlated with degree of apathy. CONCLUSIONS—This study demonstrates that DLPFC injury selectively impairs the natural tendency to seek stimulation from novel and unusual stimuli. These data provide the first quantitative behavioural demonstration that the human frontal lobes play a critical part in directing and sustaining attention to novel events. The impairment of novelty seeking behaviour may contribute to the characteristic apathy found in patients with frontal lobe injury.
Full Text
The Full Text of this article is available as a PDF (213.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- BUTTER C. M. HABITUATION OF RESPONSES TO NOVEL STIMULI IN MONKEYS WITH SELECTIVE FRONTAL LESIONS. Science. 1964 Apr 17;144(3616):313–315. doi: 10.1126/science.144.3616.313. [DOI] [PubMed] [Google Scholar]
- Baudena P., Halgren E., Heit G., Clarke J. M. Intracerebral potentials to rare target and distractor auditory and visual stimuli. III. Frontal cortex. Electroencephalogr Clin Neurophysiol. 1995 Apr;94(4):251–264. doi: 10.1016/0013-4694(95)98476-o. [DOI] [PubMed] [Google Scholar]
- Courchesne E., Hillyard S. A., Galambos R. Stimulus novelty, task relevance and the visual evoked potential in man. Electroencephalogr Clin Neurophysiol. 1975 Aug;39(2):131–143. doi: 10.1016/0013-4694(75)90003-6. [DOI] [PubMed] [Google Scholar]
- Daffner K. R., Mesulam M. M., Cohen L. G., Scinto L. F. Mechanisms underlying diminished novelty-seeking behavior in patients with probable Alzheimer's disease. Neuropsychiatry Neuropsychol Behav Neurol. 1999 Jan;12(1):58–66. [PubMed] [Google Scholar]
- Daffner K. R., Mesulam M. M., Scinto L. F., Cohen L. G., Kennedy B. P., West W. C., Holcomb P. J. Regulation of attention to novel stimuli by frontal lobes: an event-related potential study. Neuroreport. 1998 Mar 30;9(5):787–791. doi: 10.1097/00001756-199803300-00004. [DOI] [PubMed] [Google Scholar]
- Daffner K. R., Scinto L. F., Weintraub S., Guinessey J. E., Mesulam M. M. Diminished curiosity in patients with probable Alzheimer's disease as measured by exploratory eye movements. Neurology. 1992 Feb;42(2):320–328. doi: 10.1212/wnl.42.2.320. [DOI] [PubMed] [Google Scholar]
- Daffner K. R., Scinto L. F., Weintraub S., Guinessey J., Mesulam M. M. The impact of aging on curiosity as measured by exploratory eye movements. Arch Neurol. 1994 Apr;51(4):368–376. doi: 10.1001/archneur.1994.00540160062009. [DOI] [PubMed] [Google Scholar]
- FRENCH G. M., HARLOW H. F. Locomotor reaction decrement in normal and brain-damaged Rhesus monkeys. J Comp Physiol Psychol. 1955 Dec;48(6):496–501. doi: 10.1037/h0047137. [DOI] [PubMed] [Google Scholar]
- Folstein M. F., Folstein S. E., McHugh P. R. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975 Nov;12(3):189–198. doi: 10.1016/0022-3956(75)90026-6. [DOI] [PubMed] [Google Scholar]
- GLASER E. M., GRIFFIN J. P. Influence of the cerebral cortex on habituation. J Physiol. 1962 Mar;160:429–445. doi: 10.1113/jphysiol.1962.sp006857. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Halgren E., Baudena P., Clarke J. M., Heit G., Marinkovic K., Devaux B., Vignal J. P., Biraben A. Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal lobe. Electroencephalogr Clin Neurophysiol. 1995 Apr;94(4):229–250. doi: 10.1016/0013-4694(95)98475-n. [DOI] [PubMed] [Google Scholar]
- Humphrey N. K. 'Interest' and 'pleasure': two determinants of a monkey's visual preferences. Perception. 1972;1(4):395–416. doi: 10.1068/p010395. [DOI] [PubMed] [Google Scholar]
- Hutton J. T., Johnston C. W., Shapiro I., Pirozzolo F. J. Oculomotor programming disturbances in the dementia syndrome. Percept Mot Skills. 1979 Aug;49(1):312–314. doi: 10.2466/pms.1979.49.1.312. [DOI] [PubMed] [Google Scholar]
- Knight R. T. Decreased response to novel stimuli after prefrontal lesions in man. Electroencephalogr Clin Neurophysiol. 1984 Feb;59(1):9–20. doi: 10.1016/0168-5597(84)90016-9. [DOI] [PubMed] [Google Scholar]
- Knight R. T., Nakada T. Cortico-limbic circuits and novelty: a review of EEG and blood flow data. Rev Neurosci. 1998;9(1):57–70. doi: 10.1515/revneuro.1998.9.1.57. [DOI] [PubMed] [Google Scholar]
- Knight R. T., Scabini D. Anatomic bases of event-related potentials and their relationship to novelty detection in humans. J Clin Neurophysiol. 1998 Jan;15(1):3–13. doi: 10.1097/00004691-199801000-00003. [DOI] [PubMed] [Google Scholar]
- Knight R. Contribution of human hippocampal region to novelty detection. Nature. 1996 Sep 19;383(6597):256–259. doi: 10.1038/383256a0. [DOI] [PubMed] [Google Scholar]
- Kosslyn S. M., Alpert N. M., Thompson W. L., Chabris C. F., Rauch S. L., Anderson A. K. Identifying objects seen from different viewpoints. A PET investigation. Brain. 1994 Oct;117(Pt 5):1055–1071. doi: 10.1093/brain/117.5.1055. [DOI] [PubMed] [Google Scholar]
- Loftus G. R., Mackworth N. H. Cognitive determinants of fixation location during picture viewing. J Exp Psychol Hum Percept Perform. 1978 Nov;4(4):565–572. doi: 10.1037//0096-1523.4.4.565. [DOI] [PubMed] [Google Scholar]
- Marin R. S., Biedrzycki R. C., Firinciogullari S. Reliability and validity of the Apathy Evaluation Scale. Psychiatry Res. 1991 Aug;38(2):143–162. doi: 10.1016/0165-1781(91)90040-v. [DOI] [PubMed] [Google Scholar]
- Marin R. S. Differential diagnosis and classification of apathy. Am J Psychiatry. 1990 Jan;147(1):22–30. doi: 10.1176/ajp.147.1.22. [DOI] [PubMed] [Google Scholar]
- Mesulam M. M. From sensation to cognition. Brain. 1998 Jun;121(Pt 6):1013–1052. doi: 10.1093/brain/121.6.1013. [DOI] [PubMed] [Google Scholar]
- Mesulam M. M. Frontal cortex and behavior. Ann Neurol. 1986 Apr;19(4):320–325. doi: 10.1002/ana.410190403. [DOI] [PubMed] [Google Scholar]
- Morris J. C., Heyman A., Mohs R. C., Hughes J. P., van Belle G., Fillenbaum G., Mellits E. D., Clark C. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology. 1989 Sep;39(9):1159–1165. doi: 10.1212/wnl.39.9.1159. [DOI] [PubMed] [Google Scholar]
- Nelson H. E., O'Connell A. Dementia: the estimation of premorbid intelligence levels using the New Adult Reading Test. Cortex. 1978 Jun;14(2):234–244. doi: 10.1016/s0010-9452(78)80049-5. [DOI] [PubMed] [Google Scholar]
- Noton D., Stark L. Eye movements and visual perception. Sci Am. 1971 Jun;224(6):35–43. [PubMed] [Google Scholar]
- Shenton M. E., Kikinis R., Jolesz F. A., Pollak S. D., LeMay M., Wible C. G., Hokama H., Martin J., Metcalf D., Coleman M. Abnormalities of the left temporal lobe and thought disorder in schizophrenia. A quantitative magnetic resonance imaging study. N Engl J Med. 1992 Aug 27;327(9):604–612. doi: 10.1056/NEJM199208273270905. [DOI] [PubMed] [Google Scholar]
- Starkstein S. E., Fedoroff J. P., Price T. R., Leiguarda R., Robinson R. G. Apathy following cerebrovascular lesions. Stroke. 1993 Nov;24(11):1625–1630. doi: 10.1161/01.str.24.11.1625. [DOI] [PubMed] [Google Scholar]
- Vurpillot E. The development of scanning strategies and their relation to visual differentiation. J Exp Child Psychol. 1968 Dec;6(4):632–650. doi: 10.1016/0022-0965(68)90108-2. [DOI] [PubMed] [Google Scholar]
- ZUNG W. W. A SELF-RATING DEPRESSION SCALE. Arch Gen Psychiatry. 1965 Jan;12:63–70. doi: 10.1001/archpsyc.1965.01720310065008. [DOI] [PubMed] [Google Scholar]