4.2. Hippocampus (HPC)
The hippocampus is known to play a critical role in learning, as well as
the consolidation of memories during sleep (Dudai 2004). Network
connectivity between the NAcc and the hippocampus may also play an
important role in mediating the effects of SD on reward-related behavior
and motivation. The encoding of memory by the hippocampus depends on the
reactivation of specific experience-related neural firing sequences
during NREM sleep, and if this neuronal replay is interrupted by sleep
loss it impairs the subsequent recall of spatial and contextual memories
(Chen and Wilson 2017). A similar process of spontaneous replay has been
observed in the ventral striatum during NREM sleep following performance
of a reward-related task (Ahmed et al. 2008; Lansink et al. 2008;
Pennartz et al. 2004), and this reactivation is critical for the
encoding of reward-related memories, such as the spatial location of
food reward (Lansink et al. 2012). Replay sequences in the NAcc can be
triggered by sharp wave ripples in the hippocampus (Singer and Frank
2009) and replay in the NAcc is dominated by pairs of neurons in which
hippocampal “place” cells fire immediately before the reward-related
NAcc neuron (Lansink et al. 2009). Therefore, joint reactivation of
hippocampal and NAcc firing patterns represents an important mechanism
for consolidation of place-reward associations, and may be particularly
vulnerable to disruption by SD.
Reward encoding can also take place within the hippocampus itself. Place
cell firing fields accumulate near goal locations (Hollup et al. 2001),
and there are dedicated populations of neurons in the HPC that
specifically encode proximity to reward (Gauthier and Tank 2018). The
ventral region of the HPC plays a particularly important role in reward
processing. The ventral HPC sends prominent glutamatergic projections to
the NAcc which are responsible for carrying spatial information to the
NAcc and are critical for linking reward learning with contextual
information (Britt et al. 2012; Lansink et al. 2008; Lansink et al.
2009). For example, the learning of context-drug associations
selectively strengthens the connection between ventral HPC place cells
and medium spiny neurons in the NAcc (Sjulson et al. 2018), and
disruption of this pathway by inactivation of the ventral (but not
dorsal) HPC impairs the retrieval of contextual reward memory (Riaz et
al. 2017).
The ventral HPC also plays an important role in sign-tracking. One study
found that lesions of the ventral HPC, but not dorsal HPC, impaired the
initial learning of a sign-tracking response (Fitzpatrick et al. 2016a).
In another study, STs were found to have elevated myo-inositol (a marker
of glial activity and proliferation) in the ventral (but not dorsal) HPC
relative to GTs (Fitzpatrick et al. 2016b). Therefore, individual
differences in the HPC inputs to the NAcc could be a contributing factor
in the development of ST versus GT behavioral responses. It is possible
that differences in hippocampal ripple-triggered activity in the NAcc
during sleep may play a critical role in how some individuals develop
stronger incentive motivational associations with reward cues than
others. Examination of this connection in the ST/GT model would be a
critical first step in understanding the importance of the HPC in the
attribution of incentive salience to cues.