Hippocampal function and visual object processing
in temporal lobe epilepsy
M. Vannucci,
1,2,CA
Th. Dietl,
1
N. Pezer,
1
M. P. Viggiano,
2
C. Helmstaedter,
1
C. Schaller,
3
C. E. Elger
1
and Th. Grunwald
1,4
1
Departments of Epileptology and
3
Neurosurgery, University of Bonn, Germany;
2
Department of Psychology, University of Florence, via S Niccolo' 93,
50125 Firenze, Italy;
4
Swiss Epilepsy Center, Zurich, Switzerland
CA,2
Corresponding Author: manila.vannucci@psico.uni¢.it
Received 29 December 2002; accepted14 January 2003
DOI: 10.1097/01.wnr.0000079895.11980.23
Limbic event-related potentials related to verbal but not to visual
recognition memory have been found to be attenuated within the
epileptic hippocampus of patients with temporal lobe epilepsy
(TLE). To identify hippocampal contributions to visual processing
and memory we recorded intracranial ERPs directly from within
the epileptic and the non-epileptic hippocampus in 12 patients with
unilateral TLE during a visual object decision and naming task.
While the non-epileptic hippocampus di¡erentiated reliably
between real and nonsense objects, this e¡ect was completely
eliminated within the epileptic mesial temporal lobe. This ¢nding
suggests that the hippocampus proper contributes to the semantic
processing of visual objects and may help to explain visual memory
de¢cits in TLE. NeuroReport 14 :1489^1492 c 2003 Lippincott
Williams & Wilkins.
Key words: Epilepsy; Event-related potentials; Hippocampus; Temporal lobe epilepsy; Visual object processing
INTRODUCTION
The occasional need to implant depth electrodes into the
medial temporal lobes of patients with temporal lobe
epilepsy (TLE) undergoing evaluation for possible epilepsy
surgery makes it possible to record event-related potentials
(ERPs) directly from hippocampal and parahippocampal
limbic structures. It has been known for a long time that
these medial temporal brain regions play a crucial role in
declarative memory processes [1–3]. However, the possi-
bility of correlating depth ERPs with the graded memory
deficits of TLE patients has contributed to the under-
standing of the participation of different medial temporal
lobe subregions in memory processes [4–7]. In particular, a
negative field potential peaking around 400 ms has been
recorded within the anterior medial temporal lobe (AMTL-
N400) during language and memory tasks with both words
and pictures [8–11]. This potential is generated by a
parahippocampal (entorhinal) generator [12,13] and it is
reduced in amplitude by stimulus repetition [14].
AMTL-N400 elicited by words and by pictures have been
found to be differentially affected by the epileptogenic
process in TLE patients: AMTL-N400s to first presentations
of words (new) in a continuous verbal recognition paradigm
were found to be attenuated within the epileptic temporal
lobe [4,15] so that the associated new-minus-old repetition
effect is also diminished [16,17]. These unilateral attenu-
ations of limbic ERPs proved to be very helpful in
lateralizing the epileptogenic focus predicting surgical
outcome [18].
By contrast, up to now no study could demonstrate any
effects of the epileptogenic process on the AMTL-N400
elicited by both abstract pictures [19] and pictures of
common objects [9]. This discrepancy is difficult to under-
stand since seizures originating within the non-dominant
temporal lobe are associated with non-verbal memory
deficits [20,21]. In fact, if the hippocampal memory system
contributes to the memory related processing of both verbal
and non-verbal stimuli, epileptogenicity should somehow
affect limbic ERPs elicited by figurative stimuli.
Recently, functional brain imaging and electrophysiologi-
cal studies have shown that the MTL does participate in
visual object processing tasks like object decision [22], visual
object naming [23] and categorization [24] and the specific
amount and location of the activation of MTL structures in
these tasks was affected by the meaning of the pictures:
within the left MTL, meaningful pictures of real objects
elicited a significantly higher activity than meaningless
pictures of nonsense objects [22,23].
These recent findings, together with the earlier conflicting
results in studies using non-verbal vs verbal recognition
paradigms, suggest that the hippocampal memory system
could make different contributions to the encoding of verbal
and non-verbal stimuli.
To further delineate the hippocampal participation in the
processing of non-verbal material, we recorded limbic ERPs
invasively from within the human hippocampus proper
during a visual object decision and naming task. In
particular, we aimed to identify possible effects of the
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