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The Neurobiology of Pain: Developmental Aspects MARIA FITZGERALD and SIMON BEGGS1 Department of Anatomy & Developmental Biology University College London

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The Neurobiology of Pain: Developmental Aspects MARIA FITZGERALD and SIMON BEGGS1 Department of Anatomy & Developmental Biology University College London ology of Pain Volume 7, Number 3, 2001THE NEUROSCIENTIST n REVIEW The Neurobiology of Pain: Developmental Aspects MARIA FITZGERALD and SIMON BEGGS1 Department of Anatomy & Developmental Biology University College London Invasive procedures that would be painful in children and adults are frequently performed on infants admit- ted to the neonatal intensive care unit. This article discusses sensory responses to these procedures in the immature nervous system and highlights the fact that, in addition to causing distress and delayed recovery, pain in infancy is also a developmental issue. First, the immaturity of sensory processing within the new- born spinal cord leads to lower thresholds for excitation and sensitization, therefore potentially maximizing the central effects of these tissue-damaging inputs. Second, the plasticity of both peripheral and central sensory connections in the neonatal period means that early damage in infancy can lead to prolonged structural and functional alterations in pain pathways that can last into adult life. NEUROSCIENTIST 7(3):246–257, 2001 KEY WORDS Infant pain, Pediatric pain, Hyperalgesia, Allodynia, Spinal cord, Sensory neuron, C fibers, Inflammation, Neuropathic pain, Analgesia It has been reported that a preterm infant in intensive reflex responses (Fitzgerald and others 1988b; Andrews care can undergo more than 300 invasive procedures in and Fitzgerald 1994). Spinally mediated reflexes to me- a week, many of which are tissue damaging (Barker and chanical skin stimulation are exaggerated in young in- Rutter 1995; Stevens and others 1999). The effect of fants compared with the adult, with lower thresholds these procedures on the developing sensory nervous and more synchronized, longer-lasting reflex muscle system responses is a subject of considerable recent re- contractions. This is paralleled in laboratory animals, search and has highlighted the importance of the devel- where thresholds for withdrawal from mechanical, heat, opmental aspects of pain. and chemical stimuli are also lower and responses Pain responses can be simply divided into three greater in amplitude in younger animals (Fitzgerald and types: immediate responses lasting seconds to minutes, others 1988b; Guy and Abbott 1992; Falcon and others persistent responses lasting days and weeks, and pro- 1996; Hu and others 1997; Teng and Abbott 1998; longed responses that outlast the clinical period and Marsh and others 1998a). The exaggerated spinal re- may continue for years. Current research suggests that sponses are in contrast to the facial expression response, each type is triggered by different neurobiological which is weaker in younger infants and increases with mechanisms. Here we discuss the postnatal development postnatal age (Johnston and others 1993, 1995). This of these three types of pain response and their underly- may reflect a slower onset of the affective or emotional ing developmental neurobiology. response to pain as compared with the sensory-motor response, but because little is known about the matura- The Immediate Infant Pain Response tion of central pain processes in the brainstem, thalamus, and cortex, this remains speculation. The response to invasive procedures and tissue damage such as heel lancing and venipuncture in preterm infants The Persistent Infant Pain Response— has been measured in a variety of ways, notably in Inflammation terms of crying, changes in facial expression, heart rate, respiration, sweating, body movement, hormonal re- The trauma of repeated procedures will result in local sponses (see Franck and Miaskowski 1997), and flexion inflammation and hypersensitivity, which, in adults, is characterized by an enhanced sensation of pain to a This work has been supported by the Medical Research Council, the noxious stimulus (hyperalgesia) and an abnormal sensa- Child Health Research Action Trust, and Children Nationwide, United tion of pain to previously nonnoxious stimuli Kingdom. Support from the Medical Research Council, Children Na- (allodynia). In addition, there may be spontaneous or tionwide and Action Research is gratefully acknowledged. ongoing pain (Cervero and Laird 1996). The Address correspondence to: Maria Fitzgerald, Department of Anat- hyperalgesia that follows tissue injury can be divided omy & Developmental Biology, University College London (UCL), into primary and secondary hyperalgesia. Primary Gower St, London WC1E 6BT (e-mail: [email protected]). hyperalgesia develops at the site of an injury and ap- 1. Current address: AI Virtanen Institute, University of Kuopio, Finland. pears to arise largely from peripheral nociceptor sensiti- 246 THE NEUROSCIENTIST The Neurobiology of Pain Copyright © 2001 Sage Publications ISSN 1073-8584 Fig. 1. Different ways in which early tissue damage in infancy can influence peripheral cutaneous sensory terminal structure and func- tion. While many of these changes will subside with the resolution of the inflammation, others may outlast the injury for a prolonged period. DRG = dorsal root ganglion. zation. Surrounding this is a zone of secondary value of that on the intact contralateral heel (Fitzgerald mechanical hyperalgesia and allodynia, which is pro- and others 1988). The “tenderness” is established for posed to arise from central plastic changes in spinal days and weeks in the presence of tissue damage but cord connectivity modifying CNS responsiveness to fu- can be alleviated by repeated application of ture stimuli. lignocaine-prilocaine cream (EMLA) (Fitzgerald and In very young infants, cutaneous reflex responses others 1989). This response can spread outside the become sensitized upon repeated mechanical stimula- immediate area of injury. Preterm infants that have tion even in the innocuous range. Response magnitude spent time in intensive care and have done so with increases and threshold decreases after repeated innocu- established leg injuries from repeated procedures also ous mechanical stimulation at 10-sec intervals. This show significantly lower sensory thresholds even on the effect is greatest at the 28- to 33-week postconceptional intact, contralateral foot (Andrews and Fitzgerald 1994). age group and is lost by 42 weeks (Fitzgerald and oth- The low thresholds are similar to those of much youn- ers 1988a; Andrews and Fitzgerald 1994, 1999). There ger preterm infants. Although spinal responses are sen- is also good evidence that even the youngest infants are sitized under these conditions, maturation of facial capable of displaying hypersensitivity following nox- expressions in response to heel lances are delayed by ious, inflammatory stimuli. The mechanical sensory frequent invasive procedures (Johnston and Stevens reflex threshold of preterm infants in an area of local 1996). Recently, a striking hypersensitivity has been tissue damage created by repeated heel lances is half the observed in preliminary studies in postsurgical infants Volume 7, Number 3, 2001 THE NEUROSCIENTIST 247 less than 1 year old, where abdominal surgery leads to a Advances in the developmental neurobiology of fall in the sensory reflex thresholds in the wound area peripheral and spinal mechanisms of somatosensory and surrounding hyperalgesia (Andrews and others processing and pain have opened new avenues of 2000). research in infant pain. Below, we discuss possible neu- Behavioral responses to persistent inflammatory pain ral mechanisms for immediate, persistent, and pro- have not been fully examined in young rat pups. The longed infant pain. hyperalgesia or drop in mechanical threshold that fol- lows carageenan injection (Marsh and others 1998b) The Neurobiology of Infant Tissue and mustard oil application (Jiang and Gebhart 1998) is Damage—Peripheral Effects smaller in amplitude in postnatal day 3 (P3) rat neo- nates than at P21. This may be a reflection of the high Repeated tissue damage in newborn infants will natu- level of background sensitivity of young rats, which rally activate primary sensory neurons in the skin and limits the degree of hypersensitivity that they can dis- underlying tissues. In many ways, these afferents re- play. Nevertheless, it is possible to demonstrate a clear spond in a similar way to those of adults. In the rat pup, enhancement of amplitude and duration of the flexion C-fiber polymodal nociceptors, responding to mechani- reflex (de Lima and others 2000) and of dorsal horn cell cal, thermal, and chemical noxious stimuli, have mature responses (Torsney and others 2000) following thresholds and firing patterns at birth. High-threshold carageenan injection from P3. Aδ mechanoreceptors are less mature, and low-thresh- old, rapidly adapting Aβ mechanoreceptors responding The Prolonged Infant Pain Response— to touch or brush are, relatively, the most immature at Beyond the Clinical Period birth, with lower frequencies of firing and response am- plitudes than those of adults (Fitzgerald 1987; Fitzger- Sensitization to early injury may last even longer than ald and Fulton 1992). At 2 weeks of age, mice A fibers the period of clinical care. The most notable example of still have reduced conduction velocities and immature this is the observation that circumcised infants display a stimulus-response functions (Koltzenburg and others stronger pain response to subsequent routine vaccination 1997). at 4 and 6 months than uncircumcised infants. This ef- Local consequences of inflammation include the fect is attenuated by preoperative treatment with release of algogenic substances from damaged cells, lidocaine-prilocaine cream
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