On the co‐occurrence of startles and hippocampal sharp waves in newborn rats

Abstract

Hippocampal sharp waves (SPWs) are among the earliest neural population patterns observed in infant mammals. Similarly, startles are among the earliest behavioral events observed. Here we provide evidence indicating that these two events are linked mechanistically soon after birth in freely moving and head-fixed 1-4-day-old rats. EMG electrodes and intrahippocampal silicon depth electrodes were used to detect the presence of startles and SPWs, respectively. In intact pups, the majority of sharp waves were preceded by startles (average latency: 161 ms). When the hippocampal formation was surgically separated from the brainstem, however, sharp waves and startles still occurred, but now independently. In addition, unrelated to startles or SPWs, gamma oscillations were detected in several subjects, as were neocortical "spindles" that propagated passively into the hippocampus. The co-occurrence of sharp waves and startles provides the opportunity for Hebbian changes in synaptic efficacy and, thus, is poised to contribute to the assembly of neural circuits early in development.

A Triplet Repeat Expansion Genetic Mouse Model of Infantile Spasms Syndrome, Arx(GCG)10+7, with Interneuronopathy, Spasms in Infancy, Persistent Seizures, and Adult Cognitive and Behavioral Impairment

“…Startles are sudden, spontaneous, and simultaneous contractions of skeletal muscles throughout the body and have been defined behaviorally as “abrupt, high-amplitude, synchronous movements of at least three limbs” (Karlsson et al, 2006). We designed a ‘littermate array’ for our behavioral videomonitoring studies to reproducibly sample and analyze aberrant motor movements; pups were placed unrestrained in separate wells of a transparent plate that allowed full range of motion and simultaneous observation of all littermates under the same temperature-controlled conditions (Fig.…”

“…A 30-min recording in which the least voluntary movement occurred was reviewed pup by pup to score spontaneous movements during sleep and at the moment of awakening. Movements in three categories were counted: a) high-amplitude movements included rapid, abrupt displacements of the entire body across the floor of the compartment, as well as b) startles, defined as “sudden, spontaneous and simultaneous contractions of skeletal muscles throughout the body” (Karlsson et al, 2006) which displayed abdominal contractions bowing or twisting the body or as simultaneous strong movements of three or more appendages, and c) low-amplitude movements included myoclonic twitches and kicks. Voluntary movements during obvious wakefulness were not scored.…”

Spontaneous activity in the developing gerbil auditory cortex in vivo involves GABAergic transmission

“…Their incidence ranges from very slow to ultra-fast (< 0.01 Hz to >1 kHz) and reflect properties of neuronal populations interconnected by electrical and chemical synapses (Shatz, 1990; Wong, 1999; Garaschuk et al, 2000; Hirase et al, 2004; Adelsberger et al, 2005; Buzsaki, 2006; Karlsson et al, 2006; Watt et al, 2009; Tritsch and Bergles, 2010; Gonzalez-Islas and Wenner, 2010; Conhaim et al 2011; Sanes et al, 2011). In this study, repetitive occurrence of SO within the ACx in vivo during the first postnatal week (Fig.…”

“…In newborn brain slice preparations of the neocortex and hippocampus, spontaneous activity and calcium waves self-propagate across cell ensembles involving all layers, as assessed by paired recordings and two-photon fluorescent imaging. Thus, such SOs have been characterized as cortical early network oscillations (Garaschuk et al 2000), sharp waves (Karlsson et al, 2006); oscillations and waves (Kotak et al, 2007), spontaneous synchronized activity (McCabe et al, 2007), spindle burst oscillations (Minlebaev et al, 2007) or spontaneous network activity (Gonzalez-Islas and Wenner, 2010). Comparable activity has been also recorded in the neuronal and glial ensembles of postnatal mouse and rat neocortex, and cerebellum in vivo under different physiological states (Hirase et al, 2004; Adelsberger et al, 2005; Watt et al, 2009).…”

Cortical Development, Electroencephalogram Rhythms, and the Sleep/Wake Cycle

“…Startles are among the first behavioral events recorded in human fetuses and neonatal rats and consist of sudden, spontaneous and simultaneous contractions of muscles throughout the body. Although rare (1–2/min) startles occur in all behavioral states, and thus are not a unique feature of quiet sleep (20). Active sleep, by contrast, is uniquely characterized by frequent myoclonic twitches of isolated muscles that occur on a background of muscle atonia.…”