Skip to main content
SpringerLink
Log in

Comparable fMRI activity with differential behavioural performance on mental rotation and overt verbal fluency tasks in healthy men and women

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

To explicate the neural correlates of sex differences in visuospatial and verbal fluency tasks, we examined behavioural performance and blood-oxygenation-level-dependent (BOLD) regional brain activity, using functional magnetic resonance imaging, during a three-dimensional (3D) mental rotation task and a compressed sequence overt verbal fluency task in a group of healthy men (n=9) and women (n=10; tested during the low-oestrogen phase of the menstrual cycle). Men outperformed women on the mental rotation task, and women outperformed men on the verbal fluency task. For the mental rotation task, men and women activated areas in the right superior parietal lobe and the bilateral middle occipital gyrus in association with the rotation condition. In addition, men activated the left middle temporal gyrus and the right angular gyrus. For verbal fluency, men activated areas in the bilateral superior frontal gyrus, right cingulate gyrus, left precentral gyrus, left medial frontal gyrus, left inferior frontal gyrus, thalamus, left parahippocampal gyrus and bilateral lingual gyrus, and women activated areas in the bilateral inferior frontal gyrus and left caudate. Despite observing task related activation in the hypothesised areas in men and women, no areas significantly differentiated the two sexes. Our results demonstrate comparable brain activation in men and women in association with mental rotation and verbal fluency function with differential performance, and provide support for sex differences in brain–behaviour relationships.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alivisatos B, Petrides M (1997) Functional activation of the human brain during mental rotation. Neuropsychologia 35:111–118

    Article  PubMed  CAS  Google Scholar 

  • Barch DM, Braver TS, Sabb FW, Noll DC (2000) Anterior cingulate and the monitoring of response conflict: evidence from an fMRI study of overt verb generation. J Cogn Neurosci 12:298–309

    Article  PubMed  CAS  Google Scholar 

  • Barnes J, Howard RJ, Senior C, Brammer M, Bullmore ET, Simmons A, Woodruff P, David AS (2000) Cortical activity during rotational and linear transformations. Neuropsychologia 38:1148–1156

    Article  PubMed  CAS  Google Scholar 

  • Benton AL, Hamsher K (1978) Multilingual aphasia examination. University of Iowa Hospitals, IA

  • Benton AL, Hamsher KD, Varney NR, Spreen O (1983) Contributions to neuropsychological assessment: a clinical manual. Oxford University Press, New York

    Google Scholar 

  • Berman RA, Colby CL, Genovese CR, Voyvodic JT, Luna B, Thulborn KR, Sweeney JA (1999) Cortical networks subserving pursuit and saccadic eye movements in humans: an fMRI study. Hum Brain Mapp 8:209–225

    Article  PubMed  CAS  Google Scholar 

  • Buckner RL, Raichle ME, Petersen SE (1995) Dissociation of human prefrontal cortical areas across different speech production tasks and gender groups. J Neurophysiol 74:2163–2173

    PubMed  CAS  Google Scholar 

  • Canli T, Desmond JE, Zhao Z, Gabrieli JD (2002) Sex differences in the neural basis of emotional memories. Proc Natl Acad Sci USA 99:10789—10794

    Article  PubMed  CAS  Google Scholar 

  • Cohen MS, Kosslyn SM, Breiter HC, DiGirolamo GJ, Thompson WL, Anderson AK, Bookheimer SY, Rosen BR, Belliveau JW (1996) Changes in cortical activity during mental rotation: a mapping study using functional MRI. Brain 119:89—100

    Article  PubMed  Google Scholar 

  • Corballis MC (1997) Mental rotation and the right hemisphere. Brain Lang 57:100–121

    Article  PubMed  CAS  Google Scholar 

  • Cuenod CA, Bookheimer SY, Hertz-Pannier L, Zeffiro TA, Theodore WH, Le Bihan D (1995) Functional MRI during word generation, using conventional equipment: a potential tool for language localization in the clinical environment. Neurology 45:1821–1827

    PubMed  CAS  Google Scholar 

  • Curtis VA, Bullmore ET, Brammer MJ, Wright IC, Williams SC, Morris RG, Sharma TS, Murray RM, McGuire PK (1998) Attenuated frontal activation during a verbal fluency task in patients with schizophrenia. Am J Psychiat 155:1056–1063

    PubMed  CAS  Google Scholar 

  • Dabbs JM Jr (1993) Salivary testosterone measurements in behavioral studies. Ann NY Acad Sci 20:177–183

    Article  Google Scholar 

  • Dietrich T, Krings T, Neulen J, Willmes K, Erberich S, Thron A, Sturm W (2001) Effects of blood estrogen level on cortical activation patterns during cognitive activation as measured by functional MRI. Neuroimage 13:425–432

    Article  PubMed  CAS  Google Scholar 

  • Fiez JA (1997) Phonology, semantics, and the role of the left inferior prefrontal cortex. Hum Brain Mapp 5:79–83

    Article  PubMed  CAS  Google Scholar 

  • Fink G, Summer BE, McQueen JK, Wilson H, Rosie R (1998) Sex steroid control of mood, mental state and memory. Clin Exp Pharmacol Physiol 25:764–775

    Article  PubMed  CAS  Google Scholar 

  • Friedman L, Kenny JT, Wise AL, Wu D, Stuve TA, Miller DA, Jesberger JA, Lewin JS (1998) Brain activation during silent word generation evaluated with functional MRI. Brain Lang 64:231—256

    Article  PubMed  CAS  Google Scholar 

  • Friston KJ, Frith CD, Fletcher P, Liddle PF, Frackowiak RS (1996) Functional topography: multidimensional scaling and functional connectivity in the brain. Cereb Cortex 6:156–164

    Article  PubMed  CAS  Google Scholar 

  • Frith CD, Friston KJ, Liddle PF, Frackowiak RS (1991) A PET study of word finding. Neuropsychologia 29:1137–1148

    Article  PubMed  CAS  Google Scholar 

  • Frost JA, Binder JR, Springer JA, Hammeke TA, Bellgowan PSF, Rao SM, Cox RW (1999) Language processing is strongly left lateralised in both sexes: evidence from functional MRI. Brain 122:199–208

    Article  PubMed  Google Scholar 

  • Fu CH, Morgan K, Suckling J, Williams SC, Andrew C, Vythelingum GN, McGuire PK (2002) A functional magnetic resonance imaging study of overt letter verbal fluency using a clustered acquisition sequence: greater anterior cingulate activation with increased task demand. Neuroimage 17:871–879

    Article  PubMed  Google Scholar 

  • Gitelman DR, Nobre AC, Parrish TB, LaBar KS, Kim YH, Meyer JR, Mesulam M (1999) A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. Brain 122:1093–1106

    Article  PubMed  Google Scholar 

  • Gur RC, Alsop D, Glahn D, Petty R, Swanson RL, Maldjian JA, Tureksky BI, Detre JA, Gee J, Gur RE (2000) An fMRI study of sex differences in regional activation to a verbal and a spatial task. Brain Lang 74:157–170

    Article  PubMed  CAS  Google Scholar 

  • Halpern DF (1992) Sex differences in cognitive abilities, 2nd edn. Erlbaum, Hillsdale, NJ

    Google Scholar 

  • Halpern DF, Tan U (2001) Stereotypes and steroids: using a psychobiosocial model to understand cognitive sex differences. Brain Cogn 45:392–414

    Article  PubMed  CAS  Google Scholar 

  • Hampson E (1990) Estrogen-related variations in human spatial and articulatory-motor skills. Psychoneuroendocrinology 15:97–111

    Article  PubMed  CAS  Google Scholar 

  • Harris IM, Egan GF, Sonkkila C, Tochon-Danguy HJ, Paxinos G, Watson JD (2000) Selective right parietal lobe activation during mental rotation: a parametric PET study. Brain 123:65–73

    Article  PubMed  Google Scholar 

  • Hausmann M, Slabbekoorn D, VanGoozen SHM, Cohen-Kettenis PT, Gunturkun O (2000) Sex hormones affect spatial abilities during the menstrual cycle. Behav Neurosci 114:1245–1250

    Article  PubMed  CAS  Google Scholar 

  • Hutchinson M, Schiffer W, Joseffer S, Liu A, Schlosser R, Dikshit S, Goldberg E, Brodie JD (1999) Task-specific deactivation patterns in functional magnetic resonance imaging. Magn Reson Imaging 17:1427–1436

    Article  PubMed  CAS  Google Scholar 

  • Indefrey P, Levelt WJM (2000) The neural correlates of language production. In: Gazzaniga MS (eds) The new cognitive neurosciences, 2nd edn. MIT Press, Cambridge, pp 845–865

    Google Scholar 

  • Jaeger JJ, Lockwood AH, Van Valin RD Jr, Kemmerer DL, Murphy BW, Wack DS (1998) Sex differences in brain regions activated by grammatical and reading tasks. Neuroreport 9:2803–2807

    Article  PubMed  CAS  Google Scholar 

  • Johnson MD, Ojemann GA (2000) The role of the human thalamus in language and memory: evidence from electrophysiological studies. Brain Cogn 42:218–430

    Article  PubMed  CAS  Google Scholar 

  • Jordan K, Heinze HJ, Lutz K, Kanowski M, Jancke L (2001) Cortical activations during the mental rotation of different visual objects. NeuroImage 13:143–152

    Article  PubMed  CAS  Google Scholar 

  • Jordan K, Wustenberg T, Heinze HJ, Peters M, Jancke L (2002) Women and men exhibit different cortical activation patterns during mental rotation tasks. Neuropsychologia 40:2397–2408

    Article  PubMed  Google Scholar 

  • Jordan K, Schadow J, Wuestenberg T, Heinze HJ, Jancke L (2004) Different cortical activations for subjects using allocentric or egocentric strategies in a virtual navigation task. NeuroReport 15:135–140

    Article  PubMed  Google Scholar 

  • Kansaku K, Yamaura A, Kitazawa S (2000) Sex differences in lateralisation revealed in the posterior language areas. Cerebral Cortex 10:866–872

    Article  PubMed  CAS  Google Scholar 

  • Kapur S, Rose R, Liddle PF, Zipursky RB, Brown GM, Stuss D, Houle S, Tulving E (1994) The role of the left prefrontal cortex in verbal processing: semantic processing or willed action? NeuroReport 5:2193–2196

    Article  PubMed  CAS  Google Scholar 

  • Kim YH, Gitelman DR, Nobre AC, Parrish TB, LaBar KS, Mesulam MM (1999) The large-scale neural network for spatial attention displays multifunctional overlap but differential asymmetry. Neuroimage 9:269–277

    Article  PubMed  CAS  Google Scholar 

  • Kimura D (1999) Sex and cognition. The MIT Press, MA

    Google Scholar 

  • Kosslyn SM, Digirolamo GJ, Thompson WL, Alpert NM (1998) Mental rotation of objects versus hands: neural mechanisms revealed by positron emission tomography. Psychophysiology 35:151–161

    Article  PubMed  CAS  Google Scholar 

  • Lezak MD (1995) Neuropsychological assessment, 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Linn MC, Petersen AC (1985) Emergence and characterisation of sex differences in spatial ability: a meta-analysis. Child Dev 56:1479–1498

    Article  PubMed  CAS  Google Scholar 

  • Lurito JT, Kareken DA, Lowe MJ, Chen SH, Mathews VP (2000) Comparison of rhyming and word generation with fMRI. Hum Brain Mapp 10:99–106

    Article  PubMed  CAS  Google Scholar 

  • Maccoby EE, Jacklin CN (1974) The psychology of sex differences. Stanford University Press, CA

    Google Scholar 

  • Maki PM, Resnick SM (2001) Effects of estrogen on patterns of brain activity at rest and during cognitive activity: a review of neuroimaging studies. Neuroimage 14:789–801

    Article  PubMed  CAS  Google Scholar 

  • McCarthy G, Blamire AM, Rothman DL, Gruetter R, Shulman RG (1993) Echo-planar magnetic resonance imaging studies of frontal cortex activation during word generation in humans. Proc Natl Acad Sci USA 90:4952–4956

    Article  PubMed  CAS  Google Scholar 

  • McGlone J (1980) Sex differences in human brain asymmtrey: a critical survey. Behav Brain Sci 3:215–264

    Article  Google Scholar 

  • Murphy K, Corfield DR, Guz A, Fink GR, Wise RJ, Harrison J, Adams L (1997) Cerebral areas associated with motor control of speech in humans. J Appl Physiol 83:1438–1447

    PubMed  CAS  Google Scholar 

  • Nobre AC, Gitelman DR, Dias EC, Mesulam MM (2000) Covert visual spatial orienting and saccades: overlapping neural systems. Neuroimage 11:210–216

    Article  PubMed  CAS  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the edinburgh inventory. Neuropsychologia 9:97–113

    Article  PubMed  CAS  Google Scholar 

  • O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford

    Google Scholar 

  • Paulesu E, Goldacre B, Scifo P, Cappa SF, Gilardi MC, Castiglioni I, Perani D, Fazio F (1997) Functional heterogeneity of left inferior frontal cortex as revealed by fMRI. Neuroreport 8:2011–2017

    Article  PubMed  CAS  Google Scholar 

  • Peters M, Chisholm P, Laeng B (1995) Spatial ability, student gender, and academic performance. J Eng Educ 84:69–73

    Google Scholar 

  • Phelps EA, Hyder F, Blamire AM, Shulman RG (1997) fMRI of the prefrontal cortex during overt verbal fluency. NeuroReport 8:561–565

    Article  PubMed  CAS  Google Scholar 

  • Philips K, Silverman I (1997) Differences in the relationship of menstrual cycle phase to spatial performance on two- and three-dimensional tasks. Horm Behav 32:167–175

    Article  PubMed  Google Scholar 

  • Richter W, Ugurbil K, Georgopoulos A, Kim SG (1997) Time resolved fMRI of mental rotation. NeuroReport 8:3697–3702

    PubMed  CAS  Google Scholar 

  • Rosen HJ, Ojemann JG, Ollinger JM, Petersen SE (2000) Comparison of brain activation during word retrieval done silently and aloud using fMRI. Brain Cogn 42:201–217

    Article  PubMed  CAS  Google Scholar 

  • Rueckert L, Appollonio I, Grafman J, Jezzard P, Johnson R Jr, Le Bihan D, Turner R (1994) Magnetic resonance imaging functional activation of left frontal cortex during covert word production. J Neuroimaging 4:67–70

    PubMed  CAS  Google Scholar 

  • Schlosser R, Hutchinson M, Joseffer S, Rusinek H, Saarimaki A, Stevenson J, Dewey SL, Brodie JD (1998) Functional magnetic resonance imaging of human brain activity in a verbal fluency task. J Neurol Neurosurg Psychiatry 64:492–498

    PubMed  CAS  Google Scholar 

  • Seurinck R, Vingerhoets G, de Lange FP, Achten E (2004) Does egocentric mental rotation elicit sex differences? Neuroimage 23(4):1440–1449

    Article  PubMed  CAS  Google Scholar 

  • Shaywitz BA, Shaywitz SE, Pugh KR, Constable RT, Skudlarski P, Fulbright RK, Bronen RA, Fletcher JM, Shankweiler DP, Katz L et al (1995) Sex differences in the functional organization of the brain for language. Nature 373:607–609

    Article  PubMed  CAS  Google Scholar 

  • Simmons A, Moore E, Williams SC (1999) Quality control for functional magnetic resonance imaging using automated data analysis and Shewhart charting. Magn Reson Med 41:1274–1278

    Article  PubMed  CAS  Google Scholar 

  • Tagaris GA, Kim SG, Strupp JP, Andersen P, Ugurbil K, Georgopoulos AP (1996) Quantitative relations between parietal activation and performance in mental rotation. Neuroreport 29:773–776

    Article  Google Scholar 

  • Tagaris GA, Kim SG, Strupp JP, Andersen P, Ugurbil K, Georgopoulos AP (1997) Mental rotation studied by functional magnetic resonance imaging at high field (4 Tesla): performance and cortical activation. J Cogn Neurosci 9:419–432

    Article  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New York

    Google Scholar 

  • Thomsen T, Hugdahl K, Ersland L, Barndon R, Lundervold A, Smievoll AI, Roscher BE, Sundberg H (2000) Functional magnetic resonance imaging (fMRI) study of sex differences in a mental rotation task. Med Sci Monit 6:1186–1196

    PubMed  CAS  Google Scholar 

  • Tulving E, Kapur S, Craik FI, Moscovitch M, Houle S (1994) Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proc Natl Acad Sci USA 91:2016–2020

    Article  PubMed  CAS  Google Scholar 

  • Unterrainer J, Wranek U, Staffen W, Gruber T, Ladurner G (2000) Lateralized cognitive visuospatial processing: is it primarily gender-related or due to quality of performance? A HMPAO-SPECT study. Neuropsychobiology 41:95–101

    Article  PubMed  CAS  Google Scholar 

  • Voyer D, Voyer S, Bryden MP (1995) Magnitude of sex differences in spatial abilites: a meta-analysis and consideration of critical variables. Psychol Bull 117:250–270

    Article  PubMed  CAS  Google Scholar 

  • Warburton E, Wise RJ, Price CJ, Weiller C, Hadar U, Ramsay S, Frackowiak RS (1996) Noun and verb retrieval by normal subjects. Studies with PET. Brain 119:159–179

    Article  PubMed  Google Scholar 

  • Watkins KE, Gadian DG, Vargha-Khadem F (1999) Functional and structural brain abnormalities associated with a genetic disorder of speech and language. Am J Hum Genet 65:1215–1221

    Article  PubMed  CAS  Google Scholar 

  • Weiss EM, Siedentopf C, Hofer A, Deisenhammer EA, Hoptman MJ, Kremser C, Golaszewski S, Felber S, Fleischhacker WW, Delazer M (2003) Brain activation pattern during a verbal fluency test in healthy male and female volunteers: a functional magnetic resonance imaging study. Neurosci Lett 11:191–194

    Article  CAS  Google Scholar 

  • Weschler D (1981). WAIS-R. Psychological Corporation, New York

    Google Scholar 

  • Wise R, Chollet F, Hadar U, Friston K, Hoffner E, Frackowiak R (1991) Distribution of cortical neural networks involved in word comprehension and word retrieval. Brain 114:1803–1817

    Article  PubMed  Google Scholar 

  • Yetkin FZ, Hammeke TA, Swanson SJ, Morris GL, Mueller WM, McAuliffe TL, Haughton VM (1995) A comparison of functional MR activation patterns during silent and audible language tasks. Am J Neuroradiol 16:1087–1092

    PubMed  CAS  Google Scholar 

  • Yurgelun-Todd DA, Waternaux CM, Cohen BM, Gruber SA, English CD, Renshaw PF (1996) Functional magnetic resonance imaging of schizophrenic patients and comparison subjects during word production. Am J Psychiatry 153:200–205

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Centre for Social, Genetic and Developmental Psychiatry, Institute of Psychiatry, De Crespigny Park, P.O. Box 46, London, SE5 8AF, UK

    Rozmin Halari

  2. Clinical Neuroscience Research Centre, Dartford, UK

    Tonmoy Sharma

  3. Department of Psychology, City University, London, UK

    Melissa Hines

  4. Centre for Neuroimaging Sciences, Institute of Psychiatry, London, UK

    Chris Andrew & Andy Simmons

  5. Department of Psychology, Institute of Psychiatry, London, UK

    Veena Kumari

Authors
  1. Rozmin Halari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tonmoy Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Melissa Hines
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chris Andrew
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andy Simmons
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Veena Kumari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rozmin Halari.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Halari, R., Sharma, T., Hines, M. et al. Comparable fMRI activity with differential behavioural performance on mental rotation and overt verbal fluency tasks in healthy men and women. Exp Brain Res 169, 1–14 (2006). https://doi.org/10.1007/s00221-005-0118-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-005-0118-7

Keywords

Search

Navigation