The hippocampus plays a significant role in spatial memory processing, with sex differences being prominent on various spatial tasks. This study examined sex differences in healthy adults, using functional magnetic resonance imaging (fMRI) in areas implicated in spatial processing during navigation of a virtual analogue of the Morris water-maze. There were three conditions: learning, hidden, and visible control. There were no significant differences in performance measures. However, sex differences were found in regional brain activation during learning in the right hippocampus, right parahippocampal gyrus, and the cingulate cortex. During the hidden condition, the hippocampus, parahippocampal gyrus, and cingulate cortex were activated in both men and women. Additional brain areas involved in spatial processing may be recruited in women when learning information about the environment, by utilizing external cues (landmarks) more than do men, contributing to the observed sex differences in brain activation.
Get full access to this article
View all access options for this article.
References
1.
AguirreG. K.DetreJ. A.AlsopD. C.D'EspositoM. (1996) The parahippocampus subserves topographical learning in man. Cerebral Cortex, 6, 823–829.
2.
AndreanoJ. M.CahillL. (2009) Sex influences on the neurobiology of learning and memory. Learning and Memory, 16, 248–266.
3.
AsturR. S.TaylorL. B.MamelakA. N.PhilpottL.SutherlandR. J. (2002) Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behavioural Brain Research, 132, 77–84.
4.
AsturR. S.TroppJ.SavaS.ConstableR. T.MarkusE. J. (2004) Sex differences and correlations in a virtual Morris water task, a virtual radial arm maze, and mental rotation. Behavioural Brain Research, 151, 103–115.
5.
BohbotV. D.IariaG.PetridesM. (2004) Hippocampal function and spatial memory: Evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections. Neuropsychology, 18, 418–425.
6.
BurgessN. (2008) Spatial cognition and the brain. Annals of the New York Academy of Sciences, 1124, 77–97.
7.
BurgessN.MaguireE. A.O'KeefeJ. (2002) The human hippocampus and spatial and episodic memory. Neuron, 35, 625–641.
8.
CavannaA. E.TrimbleM. R. (2006) The precuneus: A review of its functional anatomy and behavioural correlates. Brain, 129, 564–583.
9.
CohenN. J.EichenbaumH. (1993) Memory, amnesia, and the hippocampal system. Cambridge, MA: The MIT Press.
10.
DriscollI.HamiltonD. A.YeoR. A.BrooksW. M.SutherlandR. J. (2005) Virtual navigation in humans: The impact of age, sex, and hormones on place learning. Hormones and Behavior, 47, 326–335.
11.
EichenbaumH.YonelinasA. P.RanganathC. (2007) The medial temporal lobe and recognition memory. Annual Review of Neuroscience, 30, 123–152.
12.
FirstM. B.SpitzerR. L.GibbonM.WilliamsJ. B. W. (1997) Structured clinical interview for DSM–IV Axis I disorders (clinical version). Washington, DC: American Psychiatric Press.
13.
FringsL.WagnerK.QuiskeA.SchwarzwaldR.SpreerJ.HalsbandU.Schulze-BonhageA. (2006) Precuneus is involved in allocentric spatial location encoding and recognition. Experimental Brain Research, 173, 661–672.
14.
FristonK. J.FrithC. D.FrackowiakR. S.TurnerR. (1995) Characterizing dynamic brain responses with fMRI: A multivariate approach. NeuroImage, 2, 166–172.
15.
FristonK. J.FrithC. D.TurnerR.FrackowiakR. S. (1995) Characterizing evoked hemodynamics with fMRI. NeuroImage, 2, 157–165.
16.
FristonK. J.WorsleyK.FrackowiakR. S.MazziottaJ.EvansA. (1994) Assessing the significance of focal activations using their spatial extent. Human Brain Mapping, 1, 214–220.
17.
GronG.WunderlichA. P.SpitzerM.TomczakR.RiepeM. W. (2000) Brain activation during human navigation: Gender-different neural networks as substrate of performance. Nature Neuroscience, 3, 404–408.
18.
HartleyT.MaguireE. A.SpiersH. J.BurgessN. (2003) The well-worn route and the path less traveled: Distinct neural bases of route following and wayfinding in humans. Neuron, 37, 877–888.
19.
IariaG.ChenJ. K.GuarigliaC.PtitoA.PetridesM. (2007) Retrosplenial and hippocamp al brain regions in human navigation: Complementary functional contributions to the formation and use of cognitive maps. European Journal of Neuroscience, 25, 890–899.
20.
IariaG.PetridesM.DagherA.PikeB.BohbotV. D. (2003) Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: Variability and change with practice. Journal of Neuroscience, 23, 5945–5952.
21.
JanzenG.van TurennoutM. (2004) Selective neural representation of objects relevant for navigation. Nature Neuroscience, 7, 673–677.
22.
JanzenG.WeststeijnC. G. (2007) Neural representation of object location and route direction: An event-related fMRI study. Brain Research, 1165, 116–125.
23.
JarrardL. E. (1993) On the role of the hippocampus in learning and memory in the rat. Behavioral and Neural Biology, 60, 9–26.
24.
MaguireE. A. (1999) Hippocampal and parietal involvement in human topographical memory: Evidence from functional neuroimaging. In BurgessN.JefferyK. J.O'KeefeJ. (Eds.), The hippocampal and parietal foundations of spatial cognition. Oxford, UK: Oxford Univer. Press. Pp. 404–415.
25.
MaguireE. A.BurgessN.DonnettJ. G.FrackowiakR. S.FrithC. D.O'KeefeJ. (1998) Knowing where and getting there: A human navigation network. Science, 280, 921–924.
26.
MoffatS. D.KennedyK. M.RodrigueK. M.RazN. (2007) Extrahippocampal contributions to age differences in human spatial navigation. Cerebral Cortex, 17, 1274–1282.
27.
MorrisR. G.GarrudP.RawlinsJ. N.O'KeefeJ. (1982) Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681–683.
28.
OhnishiT.MatsudaH.HirakataM.UgawaY. (2006) Navigation ability dependent neural activation in the human brain: An fMRI study. Neuroscience Research, 55, 361–369.
29.
O'KeefeJ.NadelL. (1978) The hippocampus as a cognitive map. Oxford, UK: Oxford Univer. Press.
30.
ParslowD. M.RoseD.BrooksB.FlemingerS.GrayJ. A.GiampietroV.BrammerM. J.WilliamsS.GasstonD.AndrewC.VythelingumG. N.LoannouG.SimmonsA.MorrisR. G. (2004) Allocentric spatial memory activation of the hippocampal formation measured with fMRI. Neuropsychology, 18, 450–461.
31.
RauchsG.OrbanP.BalteauE.SchmidtC.DegueldreC.LuxenA.MaquetP.PeigneuxP. (2008) Partially segregated neural networks for spatial and contextual memory in virtual navigation. Hippocampus, 18, 503–518.
32.
ShipmanS. L.AsturR. S. (2008) Factors affecting the hippocampal BOLD response during spatial memory. Behavioural Brain Research, 187, 433–441.
33.
SneiderTropp J.ChrobakJ. J.QuirkM. C.OlerJ. A.MarkusE. J. (2006) Differential behavioral state-dependence in the burst properties of CA3 and CA1 neurons. Neuroscience, 141, 1665–1677.
34.
Tzourio-MazoyerN.LandeauB.PapathanassiouD.CrivelloF.EtardO.DelcroixN.MazoyerB.JoliotM. (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15, 273–289.
35.
VogtB. A.FinchD. M.OlsonC. R. (1992) Functional heterogeneity in cingulate cortex: The anterior executive and posterior evaluative regions. Cerebral Cortex, 2, 435–443.
