Mark S. Blumberg

Ultrasonic vocalizations by rat pups in the cold : an acoustic by-product of laryngeal braking ?

Isolated rat pups respond to cold exposure physiologically by increasing metabolic heat production and behaviorally by emitting ultrasound. The relationship between these 2 responses was investigated by monitoring oxygen consumption, heat production by brown adipose tissue, respiratory rate, and ultrasound production during cold exposure in pups 10-12 days of age. All 3 physiological measures increased contemporaneously with the initiation of ultrasound. Pups also exhibited a respiratory pattern characterized by the prolongation of expiratory duration in relation to inspiratory duration. Ultrasound was often detected during these prolonged expirations, suggesting that pups were using laryngeal braking. Laryngeal braking is thought to enhance oxygen uptake in the lungs. Thus, ultrasound may be an acoustic by-product of a respiratory maneuver that increases oxygen delivery to metabolically active tissues during cold exposure.

The Neural Substrates of Infant Sleep in Rats

Sleep is a poorly understood behavior that predominates during infancy but is studied almost exclusively in adults. One perceived impediment to investigations of sleep early in ontogeny is the absence of state-dependent neocortical activity. Nonetheless, in infant rats, sleep is reliably characterized by the presence of tonic (i.e., muscle atonia) and phasic (i.e., myoclonic twitching) components; the neural circuitry underlying these components, however, is unknown. Recently, we described a medullary inhibitory area (MIA) in week-old rats that is necessary but not sufficient for the normal expression of atonia. Here we report that the infant MIA receives projections from areas containing neurons that exhibit state-dependent activity. Specifically, neurons within these areas, including the subcoeruleus (SubLC), pontis oralis (PO), and dorsolateral pontine tegmentum (DLPT), exhibit discharge profiles that suggest causal roles in the modulation of muscle tone and the production of myoclonic twitches. Indeed, lesions in the SubLC and PO decreased the expression of muscle atonia without affecting twitching (resulting in “REM sleep without atonia”), whereas lesions of the DLPT increased the expression of atonia while decreasing the amount of twitching. Thus, the neural substrates of infant sleep are strikingly similar to those of adults, a surprising finding in light of theories that discount the contribution of supraspinal neural elements to sleep before the onset of state-dependent neocortical activity.

Thermoregulatory competence and behavioral expression in the young of altricial species—Revisited

The behavioral and physiological thermoregulatory capabilities of newborn and infant mammals have been studied for over half a century. Psychobiologists have noted that the infants of altricial species (e.g., rats) have physical and physiological limitations such that heat loss overwhelms heat production, thus forcing a reliance on behavioral thermoregulation for the maintenance of body temperature. Recent evidence, however, suggests that a modification of this view is justified. Specifically, throughout a range of moderately cold air temperatures, nonshivering thermogenesis by brown adipose tissue contributes significantly to the infant rats behavioral and physiological adaptations to cold challenge. Given the prominent use of altricial species for the study of infant behavior, increased understanding of the infants physiological responses to cold and the effect of thermal factors on behavior is warranted.

A DEVELOPMENTAL AND COMPONENT ANALYSIS OF ACTIVE SLEEP

A wide variety of hypotheses have been put forth that address the functional significance of active sleep. Despite the well-accepted fact that active sleep expresses itself predominantly in the perinatal period, the vast majority of these functional hypotheses are applicable largely, if not exclusively, to the adult. We build on the developmental approaches of previous researchers and propose that the individual components of active sleep (e.g., myoclonic twitches, rapid eye movements) exhibit unique developmental and phylogenetic histories and may serve independent functions in the developing organism. This dynamic perspective leads to specific experimental approaches aimed at the developmental roles of these components in the neonate, their maintenance roles in the adult, and the means by which these various components coalesce temporally in what is commonly referred to as a behavioral state.

Thermogenesis, Myoclonic Twitching, and Ultrasonic Vocalization in Neonatal Rats During Moderate and Extreme Cold Exposure

Physiological and behavioral responses of 2- and 7-8-day-old rats were monitored during moderate and extreme cold exposure. During moderate cold exposure (30 degrees C < or = air temperature < or = 32.5 degrees C), pups at both ages increased heat production, maintained an elevated interscapular temperature, and maintained baseline levels of myoclonic twitching, a behavior commonly associated with active sleep. During extreme cold exposure (21 degrees C < or = air temperature < or = 25 degrees C), pups at both ages continued producing metabolic heat, but now exhibited pronounced decreases in interscapular temperature and decreased rates of myoclonic twitching. Furthermore, the 7-8-day-old pups exhibited significant increases in ultrasound production, and males vocalized more than females. These results suggest the presence of a narrow subthermoneutral zone in neonates in which nonshivering thermogenesis is regulated and sleep-related behaviors are protected.

Rapid whisker movements in sleeping newborn rats.

Spontaneous activity in the sensory periphery drives infant brain activity and is thought to contribute to the formation of retinotopic and somatotopic maps. In infant rats during active (or REM) sleep, brainstem-generated spontaneous activity triggers hundreds of thousands of skeletal muscle twitches each day; sensory feedback from the resulting limb movements is a primary activator of forebrain activity. The rodent whisker system, with its precise isomorphic mapping of individual whiskers to discrete brain areas, has been a key contributor to our understanding of somatotopic maps and developmental plasticity. But although whisker movements are controlled by dedicated skeletal muscles, spontaneous whisker activity has not been entertained as a contributing factor to the development of this system. Here we report in 3- to 6-day-old rats that whiskers twitch rapidly and asynchronously during active sleep; furthermore, neurons in whisker thalamus exhibit bursts of activity that are tightly associated with twitches but occur infrequently during waking. Finally, we observed barrel-specific cortical activity during periods of twitching. This is the first report of self-generated, sleep-related twitches in the developing whisker system, a sensorimotor system that is unique for the precision with which it can be experimentally manipulated. The discovery of whisker twitching will allow us to attain a better understanding of the contributions of peripheral sensory activity to somatosensory integration and plasticity in the developing nervous system.

Extraocular muscle activity, rapid eye movements and the development of active and quiet sleep

Rapid eye movements (REMs), traditionally measured using the electrooculogram (EOG), help to characterize active sleep in adults. In early infancy, however, they are not clearly expressed. Here we measured extraocular muscle activity in infant rats at 3 days of age (P3), P8 and P14–15 in order to assess the ontogeny of REMs and their relationship with other forms of sleep‐related phasic activity. We found that the causal relationship between extraocular muscle twitches and REMs strengthened during the first two postnatal weeks, reflecting increased control of the extraocular muscles over eye movements. As early as P3, however, phasic bursts of extraocular muscle twitching occurred in synchrony with twitching in other muscle groups, producing waves of phasic activity interspersed with brief periods of quiescence. Surprisingly, the tone of the extraocular muscles, invisible to standard EOG measures, fluctuated in synchrony with the tone of other muscle groups; focal electrical stimulation within the dorsolateral pontine tegmentum, an area that has been shown to contain wake‐on neurons in P8 rats, resulted in the simultaneous activation of high tone in both nuchal and extraocular muscles. Finally, when state‐dependent neocortical electroencephalographic activity was observed at P14, it had already integrated fully with sleep and wakefulness as defined using electromyographic criteria alone; this finding is not consistent with the notion that active sleep in infants at this age is ‘half‐activated.’ All together, these results indicate exquisite temporal organization of sleep soon after birth and highlight the possible functional implications of homologous activational states in striated muscle and neocortex.

The union of the state: Myoclonic twitching is coupled with nuchal muscle atonia in infant rats

Active sleep (AS), as measured by the occurrence of myoclonic twitching (MT), is the most prevalent behavioral state in newborn rats. Historically, AS has been considered a developmental precursor of REM sleep, but recently this idea has been questioned. In the present study, the authors assess, in 2-, 5-, and 8-day-old rats, the relationship between MT and nuchal muscle atonia, a widely recognized component of REM sleep. At all ages, muscle atonia preceded MT and persisted until awake behaviors occurred. In addition, muscle tone decreased gradually during transitions from awake behavior to twitching. Thus, MT during infancy occurs against a backdrop of muscle atonia, a result that is consistent with the view that AS is a developmental precursor of REM sleep.

Spontaneous Motor Activity in Fetal and Infant Rats Is Organized Into Discrete Multilimb Bouts

Spontaneous motor activity (SMA) is a ubiquitous feature of fetal and infant behavior. Although SMA appears random, successive limb movements often occur in bouts. Bout organization was evident at all ages in fetal (embryonic day [E] 17-21) and infant (postnatal day [P] 1-9) rats, with nearly all bouts comprising 1-4 movements of different limbs. A computational model of SMA, including spontaneous activity of spinal motor neurons, intrasegmental and intersegmental interactions, recurrent inhibition, and descending influences, produced bouts with the same structure as that observed in perinatal rats. Consistent with the model, bouts were not eliminated on E20 after cervical spinal transection, suggesting that the brain is not necessary to produce bout organization. These investigations provide a foundation for understanding the contributions of SMA to neuromuscular and motor development.

Inter-litter competition and communal nursing among Norway rats: advantages of birth synchrony

SummaryThe effect of inter-litter competition on pup survival was investigated in pairs of female rats (Rattus norvegicus) living and breeding in the same environment. If a female gave birth when a 0- to 14-day-old litter was already present in the environment, her pups had a very high chance of surviving, similar to the situation in which no other litter was present. Moreover, the mother was likely to nurse communally with the mother of the 0- to 14-day-old litter. This communal nursing benefitted the newborn pups as evidenced by their being heavier at weaning than litters that were not nursed communally. In contrast, if a female gave birth when a 15-to 28-day-old litter was already present in the environment, her newborn pups were likely to die within 3 days postpartum, owing to the fact that they were often prevented from suckling at their mothers teats, resulting in milk deprivation, and were often beneath the older pups, resulting in physical trauma. These findings suggest that inter-litter competition is an important source of pup mortality when litters are born 15-28 days apart. The data are discussed in terms of the advantages of birth synchrony.