Abstract
The hippocampus is not a unitary, homogeneous brain area. Anatomical and functional specialization is evident along the septotemporal axis of the structure, and between the left and right hemispheres. In the mouse brain, a left–right asymmetry has been discovered in the plasticity of CA3-CA1 projections originating in the left versus right hippocampus. Presynaptic afferents originating in the left hemisphere—including both uncrossed Schaffer collaterals, and crossed commissural projections to the contralateral CA1—form small, plastic synapses, whereas afferents originating in right CA3 contact larger, less plastic, synapses. Studies using optogenetic techniques to selectively activate fibers originating from one hemisphere in ex vivo slices have revealed that projections originating from left CA3 exhibit a far greater capacity for long-term potentiation (LTP) of synaptic strength than those originating on the right. However, corresponding data from rats are currently unavailable, leaving open the question of species differences in hippocampal symmetry. In the current study, we reanalyzed data from our previous in vivo LTP work to address this issue. We analyzed plasticity in independent Schaffer collateral and commissural projections to CA1 originating from left and right CA3 in male Lister-hooded rats. However, we found no differences in the magnitude and duration of LTP induced in either crossed or uncrossed pathways following high-frequency tetanization of left versus right CA3. This contrast with previous findings may stem from methodological differences between in vivo electrical and ex vivo optogenetic approaches, but may reflect a genuine species difference in the organization and laterality of the rodent CA3-CA1 system.
Highlights
The hippocampus is a structurally and operationally heterogeneous structure
Strong tetanization of CA3 resulted in similar long-term potentiation (LTP) in all 4 pathways examined: left CA3-CA1 uncrossed Schaffer collateral (n = 10), right CA3-CA1 uncrossed Schaffer collateral (n = 16); left CA3-right CA1 crossed commissural projection (n = 12), and right CA3-left CA1 crossed commissural projection (n = 17) (Fig. 2A)
Weak tetanization of CA3 led to decaying early LTP that reached baseline within approximately 3 h in all 4 pathways: left CA3-CA1 uncrossed Schaffer collateral (n = 5), right CA3-CA1 uncrossed Schaffer collateral (n = 6); left CA3-right CA1 crossed commissural projection (n = 4), and right CA3-left CA1 crossed commissural projection (n = 8) (Fig. 3A)
Summary
The hippocampus is a structurally and operationally heterogeneous structure. There is abundant evidence for functional differentiation along the septotemporal (dorsoventral) axis (de Hoz et al, 2014; Strange et al, 2014; Bast et al, 2011), and functional imaging and neuropsychological studies have long pointed to a division of labor between the left and right hippocampus in humans, with greater right hippocampal involvement in allocentric spatial memory, and a more pronounced role for the left hippocampus in autobiographical or episodic memory (see Burgess et al, 2002). Recent work has uncovered some intriguing asymmetries in the CA1 synapses of left versus right CA3 neurons: in the apical dendrites of mouse CA1, afferents originating from the left hemisphere preferentially innervate smaller spines with a high density of NMDA GluN2B subunits—necessary for the induction of persistent LTP in vivo (Ballesteros et al, 2016)—whereas projections originating on the right tend to target larger, mushroomshaped spines, with higher densities of AMPA GluA1 receptor subunits (Kawakami et al, 2003; Wu et al, 2005; Shinohara et al, 2008; Shinohara and Hirase, 2009) This is true in both ipsilateral Schaffer collateral projections, and in contralateral commissural fibers.
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