Mamillary Body Lesions in Monkeys Impair Object-in-Place Memory: Functional Unity of the Fornix-Mamillary System

Six monkeys were trained preoperatively in an automated object-in-place memory task in which they learned 20 new scenes in each daily session. Three of the six monkeys then received stereotaxically guided bilateral mamillary body lesions, leaving the fornix intact, while the other three received a control operation. Postoperatively the control animals' rate of learning new scenes was unchanged, but the animals with mamillary body lesions showed a severe impairment, equal to that seen in previous experiments after fornix transection. All six animals were then given fornix transection, in addition to the existing mamillary or control operation. The control group now showed, after fornix transection, an impairment equal to that of the animals with mamillary body lesions alone. But the animals with mamillary body lesions did not show any additional impairment following fornix transection. We conclude that (1) the role of the mamillary bodies in a model of human episodic memory is as important as the role of the fornix, (2) the fornix and mamillary bodies form a single functional memory system, since the effect of lesions in both parts is no more severe than the effects of a lesion in one of the parts alone, and (3) the idea that the functional effects of fornix transection result from cholmergic deafferentation of the hippocampus receives no support from the present results; rather, they support the idea that in primates the fornix and mamillary bodies, together with connected structures, including the subiculum, mamillo-thalamic tract, anterior thalamic nuclei, and cingulate bundle, form a cortico-cortical association pathway for episodic memory.

[1]  J. Mikol,et al.  [Neuropathology of amnesic syndromes in man]. , 1985, Revue neurologique.

[2]  R. Ridley,et al.  Visuospatial learning impairment following lesion of the cholinergic projection to the hippocampus , 1988, Brain Research.

[3]  D. Gaffan,et al.  The Recognition Memory Deficit Caused by Mediodorsal Thalamic Lesion in Non‐human Primates: A Comparison with Rhinal Cortex Lesion , 1997, The European journal of neuroscience.

[4]  E. J. Holmes,et al.  Ablations of the mammillary nuclei in monkeys: Effects on postoperative memory , 1983, Experimental Neurology.

[5]  Jean Delay,et al.  Le Syndrome de Korsakoff , 1969 .

[6]  R. Sutherland,et al.  The role of the fornix/fimbria and some related subcortical structures in place learning and memory , 1989, Behavioural Brain Research.

[7]  J. Aggleton,et al.  Both fornix and anterior thalamic, but not mammillary, lesions disrupt delayed non-matching-to-position memory in rats , 1991, Behavioural Brain Research.

[8]  R. Wise,et al.  Mammillary Body Damage Results in Memory Impairment But Not Amnesia , 1998 .

[9]  R. Nitsch,et al.  Substance P-containing hypothalamic afferents to the monkey hippocampus: an immunocytochemical, tracing, and coexistence study , 1994, Experimental Brain Research.

[10]  L R Squire,et al.  Lesions of the hippocampal formation but not lesions of the fornix or the mammillary nuclei produce long-lasting memory impairment in monkeys , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  P. Goldman-Rakic,et al.  The primate mediodorsal (MD) nucleus and its projection to the frontal lobe , 1985, The Journal of comparative neurology.

[12]  J. Aggleton,et al.  The effects of mammillary body and combined amygdalar-fornix lesions on tests of delayed non-matching-to-sample in the rat , 1990, Behavioural Brain Research.

[13]  M. Petrides,et al.  Memory Impairments Following Lesions to the Mammillary Region of the Rat , 1993, The European journal of neuroscience.

[14]  N. Kapur,et al.  The Mammillary Bodies Revisited , 1994 .

[15]  R. Ridley,et al.  Restoration of learning ability in fornix-transected monkeys after fetal basal forebrain but not fetal hippocampal tissue transplantation , 1992, Neuroscience.

[16]  N. Kapur,et al.  The role of diencephalic pathology in human memory disorder. Evidence from a penetrating paranasal brain injury. , 1990, Brain : a journal of neurology.

[17]  D. Gaffan Episodic and semantic memory and the role of the not-hippocampus , 1997, Trends in Cognitive Sciences.

[18]  E. Greene,et al.  The role of mammillary bodies in spatial memory , 1977, Experimental Neurology.

[19]  E. J. Holmes,et al.  An examination of the effects of mammillary-body lesions on reversal learning sets in monkeys , 1983 .

[20]  J. Aggleton,et al.  A comparison of the effects of anterior thalamic, mamillary body and fornix lesions on reinforced spatial alternation , 1995, Behavioural Brain Research.

[21]  L. Jarho Korsakoff-like amnesic syndrome in penetrating brain injury. A study of Finnish war veterans. , 1973, Acta neurologica Scandinavica. Supplementum.