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«Distribution Agreement In presenting this thesis or dissertation as a partial fulfillment of the requirements for an advanced degree from Emory ...»

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(A) Time spent in open arms was significantly greater in PS animals compared to non-stressed controls (Mann-Whitney U test, U32 = 60, ** p 0.01). (B) The number of dips made on the plusmaze by PS animals was significantly higher than those made by controls (U32 = 85, * p 0.05).

(C, D) There was no effect of PS on open arm entries (C) or locomotor activity as measured by center crossings (D). 16 ≤ N ≤ 18.

Figure 5.4 PS tends to reduce ultrasonic vocalization of isolated pups during a developmental critical period.

Figure 5.4 PS tends to reduce ultrasonic vocalization of isolated pups during a developmental critical period.

(A, B) The number of USVs of the pups isolated from their litters are depicted for rats at P7 (A) and P17 (B). 7 ≤ N ≤ 12.

Figure 5.5 Sociability in adult rat offspring exposed to PS.

Figure 5.5 Sociability in adult rat offspring exposed to PS.

(A) Interaction of control and PS rats with a novel object and conspecific is depicted from the sociability test. (B) PS rats spent less time interacting with other rats in the social choice test, and did not exhibit a preference for novel rats over familiar rats (Two-way ANOVA, main effect of PS: F1,14 = 4.04, p = 0.06). (C) Preference index is plotted for PS and control rats for the sociability and social choice tests. 4 ≤ N ≤ 5.

Figure 5.6 The impact of PS on the developmental trajectory of intrinsic membrane properties of BLA principal neurons.

Figure 5.6 The impact of PS on the developmental trajectory of intrinsic membrane properties of BLA principal neurons.

(A, B) There was no difference in the age-dependent changes to input resistance (Rin, A) or membrane time constant (B) in prenatally stressed rats compared to controls. (C) Resting membrane potential (RMP) was significantly more hyperpolarized across all ages in prenatally stressed rats compared to controls (Two-way ANOVA, main effect of stress: F1,148 = 4.63, p 0.05). 7 ≤ N ≤ 19.

Figure 5.7 The developmental trajectory of action potential (AP) properties of BLA principal neurons are altered by PS.

Figure 5.7 The developmental trajectory of action potential (AP) properties of BLA principal neurons are altered by PS.

(A) AP waveforms, depicted as mean (solid line) and standard deviation (band), are shown for BLA principal neurons across postnatal development.

The same data are shown at two resolutions to depict the full waveform (top) and the AP threshold and AHP (bottom). (B) AP threshold was significantly more hyperpolarized across all ages in PS animals (Two-way ANOVA, main effect of PS: F1,146 = 5.85, p 0.05). (C) APs were significantly taller in PS animals (F1,149 = 4.62, p 0.05). (D) The peak voltage deflection of the fAHP, for neurons in which one was detected, became more hyperpolarized with age but is unaffected by PS (Main effect of PS, F1,66 = 2.34, p 0.05). (E-G) AP kinetics are plotted in terms of half-width (E), 10-90% rise time (F), and 90-10% decay time (G), but none of these metrics exhibit an effect of PS. 9 ≤ N ≤ 19.

Figure 5.8 BLA principal neuron excitability was reduced in adulthood but not during development by PS.

Figure 5.8 BLA principal neuron excitability was reduced in adulthood but not during development by PS.

(A) The rheobase was significantly greater at P60 in neurons from offspring exposed to prenatal stress (Bonferroni post-test, ** p 0.01; Two-way ANOVA, interaction effect: F5,135 = 3.24, p 0.01). (B) The maximum spike rate increased with age but was not altered by prenatal stress. (C) The current injection required to elicit the maximum spike rate was greater for BLA principal neurons from PS rats (Two-way ANOVA, main effect of stress: F1,128 = 5.32, p 0.05). (D) F-I curves are plotted for PS and control BLA principal neurons at each time point. Lines represent the mean and shaded bands represent the SEM for each group. 8 ≤ N ≤ 17.

Figure 5.9 GABAA responses in BLA principal neurons are slower during development in PS rats.

Figure 5.9 GABAA responses in BLA principal neurons are slower during development in PS rats.

(A) Schematic of recording and stimulation sites. The stimulating electrode (stim) was placed medial to the external capsule (EC) within the BLA. The lateral nucleus (LA) and central nucleus (CeA) of the amygdala are also labeled. The compass gives directions for dorsal (D), ventral (V), lateral (L), and medial (M). (B) The decay time constant of stimulation-evoked IPSCs are depicted for BLA principal neurons across postnatal development. There was a significant interaction of age and prenatal stress (Two-way ANOVA, F5,142 = 2.79, p 0.05). At P14, the decay time consant was significantly longer in neurons from prenatally stressed animals (Bonferroni post-test, * p 0.05). 5 ≤ N ≤ 20. (C, D) Representative PSCs (average of 5 sweeps) are illustrated for one PS and one control neuron at P14 (C) and P60 (D). Stimulation artifacts are cropped for clarity.

Figure 5.10 Effect of PS on short-term plasticity of GABAA PSCs.

Figure 5.10 Effect of PS on short-term plasticity of GABAA PSCs.

(A) Ratio of amplitudes of stimulation-evoked, GABAA receptor-mediated IPSCs in BLA principal neurons. The ratio of the peak amplitudes for pulse 5 and pulse 1 are depicted across postnatal development for neurons from prenatally stressed and control rats (not significant, Two-way ANOVA, main effect of stress: F1,129 = 2.59, p = 0.11). (B) Representative responses to 20hz stimulation for neurons from a prenatally stressed and control rat at P21. Stimulation artifacts were cropped for clarity. The area under the curve was filled to aid visual comparison across time points. (C) Similar to (A), ratios of the peak amplitudes of pulse 5 and pulse 1 are depicted for 50hz stimulation across postnatal development and for both groups. 2 ≤ N ≤ 9.

Figure 5.11 PS reduces BLA expression of the GABAA receptor α1 subunit beginning at P17.

Figure 5.11 PS reduces BLA expression of the GABAA receptor α1 subunit from P17 onwards.

(A) PS significantly reduced α1 subunit mRNA expression, depicted as 2-Δ ΔCt, across all ages and specifically at P21, measured using real-time RT-PCR (Bonferroni post-test, * p 0.05; Two-way ANOVA, main effect of stress: F1,20 = 14.13, p 0.01). N = 3. (B) The effect of prenatal stress on α1 subunit mRNA is also expressed as fold change relative to controls.

Figure 5.12 Schematic of the effects of prenatal stress on BLA development Figure 5.

12 Schematic of the effects of prenatal stress on BLA development. The effects of prenatal stress in the BLA are represented as approximate trajectories, including increased duration of IPSCs around P14, reduced action potential (AP) threshold and resting membrane potential throughout development, decreased expression of the GABAA receptor α1 subunit, and reduced neuronal excitability starting around P28 and persisting into adulthood. Reduced emotionality is also included, based on reduced anxiety in the elevated plus-maze, decreased sociability in the social choice test, and fewer isolation-induced ultrasonic vocalizations.

Chapter 6: Spike-Timing Precision and Neuronal Synchrony are Enhanced by an Interaction between Synaptic Inhibition and

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Adapted from Ryan SJ*, Ehrlich DE*, Jasnow AM*, Daftary S, Madsen TE, Rainnie DG (2012). Spike-timing precision and neuronal synchrony are enhanced by an interaction between synaptic inhibition and membrane oscillations in the amygdala. PLoS One 7 (4): e35320.

6.1 Abstract The basolateral complex of the amygdala (BLA) is a critical component of the neural circuit regulating fear learning. During fear learning and recall, the amygdala and other brain regions, including the hippocampus and prefrontal cortex, exhibit phase-locked oscillations in the high delta / low theta frequency band (~2-6 Hz) that have been shown to contribute to the learning process. Network oscillations are commonly generated by inhibitory synaptic input that coordinates action potentials in groups of neurons. In the rat BLA, principal neurons spontaneously receive synchronized, inhibitory input in the form of compound, rhythmic, inhibitory postsynaptic potentials (IPSPs), likely originating from burst-firing parvalbumin interneurons. Here we investigated the role of compound IPSPs in the rat and rhesus macaque BLA in regulating action potential synchrony and spike-timing precision. Furthermore, because principal neurons exhibit intrinsic oscillatory properties and resonance between 4 and 5 Hz, in the same frequency band observed during fear, we investigated whether compound IPSPs and intrinsic oscillations interact to promote rhythmic activity in the BLA at this frequency. Using whole-cell patch clamp in brain slices, we demonstrate that compound IPSPs, which occur spontaneously and are synchronized across principal neurons in both the rat and primate BLA, significantly improve spike-timing precision in BLA principal neurons for a window of ~300 ms following each IPSP. We also show that compound IPSPs coordinate the firing of pairs of BLA principal neurons, and significantly improve spike synchrony for a window of ~130 ms.

Compound IPSPs enhance a 5 Hz calcium-dependent membrane potential oscillation (MPO) in these neurons, likely contributing to the improvement in spike-timing precision and synchronization of spiking. Activation of the cAMP-PKA signaling cascade enhanced the MPO, and inhibition of this cascade blocked the MPO. We discuss these results in the context of spiketiming dependent plasticity and modulation by neurotransmitters important for fear learning, such as dopamine.

6.2 Introduction The basolateral complex of the amygdala (BLA) is a critical part of the neural circuit regulating fear learning (Miserendino et al., 1990; Campeau et al., 1992; Davis, 2000; LeDoux, 2000; Rodrigues et al., 2001), and recent evidence suggests that oscillatory activity of neurons in this region plays a key role in regulating affect in awake, behaving animals (for review, see Pape and Pare, 2010). More specifically, it is now evident that the amygdala, hippocampus, and prefrontal cortex produce coordinated high delta / low theta (4-5 Hz) oscillations during acquisition (Madsen and Rainnie, 2009) and retrieval (Sangha et al., 2009) of learned fear, which then diminish over the course of subsequent extinction learning. Significantly, phase-locked theta stimulation applied simultaneously to the amygdala and hippocampus disrupts fear extinction and prolongs the expression of learned fear (Lesting et al., 2011), further supporting a role of synchronized neural activity in the processes of fear learning and extinction. Moreover, synchronous theta oscillations during REM sleep in the period between fear acquisition and retrieval correlate with changes in fear expression, suggesting that theta oscillations are critical for successful consolidation of fear memory (Popa et al., 2010). Despite the importance of these low frequency oscillations to amygdala function and emotional learning, the mechanisms by which the BLA circuit generates rhythmic activity are largely unknown.

A common mechanism for generating network oscillations utilizes coordinated inhibitory input across multiple neurons to synchronize their action potential firing (Soltesz and Deschenes, 1993; Buzsaki, 1997; Penttonen et al., 1998; Pouille and Scanziani, 2001; Person and Perkel, 2005; Sohal et al., 2006; Szucs et al., 2009). The BLA is organized to exploit this phenomenon through the rhythmic interaction of excitatory principal neurons and inhibitory interneurons. BLA principal neurons exhibit compound, rhythmic, inhibitory postsynaptic potentials (IPSPs) that occur at a baseline frequency of 0.5-4 Hz that is sensitive to modulation by dopamine and serotonin (Rainnie, 1999b; Loretan et al., 2004; Muly et al., 2009). These rhythmic IPSPs are driven by action potentials in local, burst-firing interneurons, which we have previously shown to express parvalbumin (PV+) (Rainnie et al., 2006). PV+ interneurons have several characteristics that enable them to influence the activity of large networks of BLA principal neurons synchronously: first, these interneurons make up approximately 40% of the total interneuron population and are distributed throughout the BLA; second, each PV+ interneuron can innervate the soma and axon hillock of approximately 150 principal neurons (McDonald et al., 2005);

finally, these interneurons are coupled electrically by gap junctions to create a functional syncytium (Muller et al., 2005; Woodruff and Sah, 2007a, b). Significantly, we and others have shown that, in paired recordings of rat BLA principal neurons, spontaneous IPSPs are highly synchronized (Rainnie, 1999a; Popescu and Pare, 2011), suggesting that the output of PV+ interneurons may coordinate the activity of large numbers of principal neurons.

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