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| Figure 1 |
Work on this project is ongoing. It is already known that both amygdala
(AMG) and GC are involved in at least some forms of conditioned taste
aversion (CTA). Neurons in both areas change their chemosensory profiles
following training (Yasoshima et al 1995, Yasoshima & Yamamoto 1998), such
that the overall response magnitudes to the conditioned stimulus come to be
more in line with those to unpleasant stimuli. It also appears that either
lesions of either AMG or GC can prevent animals from acquiring CTAs (Morris
et al 1999, Yamamoto et al 1995, Yamamoto et al 1994), although this effect
may depend upon the exact behavioral paradigm used (Schafe et al 1998).
Learning is inhibited when GC is inactivated during taste presentation, or
when the AMG is inactivated during administration of LiCl (Bielavska &
Roldan 1996, Gallo et al 1998). GC also appears necessary for extinction of
previously acquired CTA (Berman & Dudai 2001). Complexities of the
connectivity between regions in the taste system make it difficult to reach
conclusions on the basis of lesion data, however. A more rigorous test of a
brain area's involvement in learning involves challenging each region's
ability to express learning-related plasticity during training (see, for
instance, Chen & Steinmetz 2000). In fact, a number of studies have
indicated that CTA does not develop when learning-related plasticity is
inhibited in either GC or AMG (Lamprecht et al 1997, Rosenblum et al 1997,
Yasoshima et al 2000, Yasoshima & Yamamoto 1997).
We have begun an in-depth analysis of the involvement of GC and AMG in CTA.
Figure 1 shows one example of a single neuron held from before until after
training (the lower panels demonstrate the consistency of isolability from
the training day to the testing day). Before learning, this neuron's firing
became inhibited following tastant administration; after learning, its
sucrose response had become excitatory. The spontaneous firing rate changed
in a direction opposing the change in evoked response, a result predicted by
recent empirical/theoretical work on plasticity (see Turrigiano 1999). Note
also that training also reduced the latency of the response from ~600 to <
100 msec; such a change could facilitate cortical involvement in speeded
responding known to appear in certain training paradigms (Boughter et al
2002, Halpern & Tapper 1971).
The fact that both GC and AMG are active, plastic, and necessary during CTA
suggests that they may work together during taste learning. Several authors
have suggested exactly this, offering data that can be interpreted as
evidence that GC and ipsilateral AMG interact to support conditioning
(Bielavska & Roldan 1996, Gallo & Bures 1991, Schafe et al 1995). As
mentioned above, the AMG is reciprocally connected to ipsilateral GC in rats
(Shi & Cassell 1998) and primates (Mesulam & Mufson 1982). Stimulation of
the AMG activates neurons and causes LTP in GC (Escobar et al 2003, Yamamoto
et al 1984), while GC stimulation increases the palatability of many
tastants (Cubero & Puerto 2000) in a manner counter to the effect of AMG
lesion (Galaverna et al 1993, Touzani et al 1997)-thus it appears that the
effects of GC stimulation have to do with the AMG-GC interconnection. As
might therefore be expected, cutting the connection between GC and AMG
impedes the retention of CTA, even if both areas are themselves left intact
(Yamamoto et al 1984).
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| Figure 2 |
If the connectivity between AMG and GC is truly important for gustatory
learning, electrophysiological recordings should show evidence of this
importance: the time-courses of GC taste responses should change with
learning (see below), as should coherence between GC and AMG. Changes in
the time-courses of neural responses are of course a ubiquitous part of
learning; recent multi-electrode data from other behavioral preparations,
meanwhile, confirms that learning may correlate with increases of coherence
between neurons in cortex (Laubach et al 2000, Schoenbaum et al 2000), or
even between connected neurons in cortical and subcortical structures
(Laubach & Nicolelis 1998). Furthermore, directionality of coherence has
been observed during olfactory recognition (Kay, Lancaster, & Freeman 1996).
Such effects are predicted and granted theoretical significance by dynamical
models of brain function (Sporns et al 2000). We have collected preliminary
data from rats implanted with both AMG and GC bundles (Figure 2), which
demonstrate that such expectations are borne out in the awake animal. In
each panel, the thin lines represent AMG-GC coherence before training, and
the thick lines represent post-training coherence. In both cases training
changed the coherence between AMG and GC, with the positive post-training
peaks lagging slightly after zero, suggesting that AMG leads GC; the lags of
maximum coherence (thin vertical lines) were similar to reported AMG-to-GC
transmission time (Yamamoto et al 1984). Decreases in coherence were never
observed.
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