How the neonatal rat gets to the nipple: Common motor modules and their involvement in the expression of early motor behavior

q 1998 John Wiley & Sons, Inc. CCC 0012-1630/98/010057-10

DEV (WILEJ) INTERACTIVE

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David EilamDepartment of Zoology

Tel-Aviv University Ramat-Aviv69 978, Israel

William P. SmothermanLaboratory of Perinatal

NeuroethologyCenter for Developmental

PsychobiologyDepartment of Psychology

State University of New YorkAt Binghamton

Binghamton, NY, 13902–6000

How the Neonatal Rat Gets to

the Nipple: Common Motor

Modules and Their

Involvement in the Expression

of Early Motor Behavior

Received 9 May 1996; accepted 13 December 1996

ABSTRACT: One-day-old rat pups adopt a supine posture before attaching to the mother’snipple. Body rotations performed to reach the nipple occur in a typical kinematic structure.First, the pup rotates along the longitudinal axis of the trunk and lies on its side. Next, the puparches the trunk to achieve a U-shaped posture and then rapidly relaxes the trunk. A secondcephalocaudal rotation follows at the peak of trunk relaxation as the pup achieves a supineposture. After reaching a supine posture, the pup crawls to a nipple by performing “stepping”movements on the mother’s ventral surface. The kinematic structure of these movements isreminiscent of the structure of righting as seen in the newborn rat. Both righting and achievinga supine posture under the mother involve the expression of common motor modules. Duringrighting the modules are executed in the direction of gravity, and when achieving a supineposture the modules are executed against the force of gravity. Simple motor behaviors expressedby the rat pup during early postnatal development may have common origins and commoncontrol mechanisms. q 1998 John Wiley & Sons, Inc. Dev Psychobiol 32: 57–66, 1998

Keywords: motor behavior; suckling; righting; pivoting; punting; maternal behavior

While weanling-age rodents appear to exhibit a motorrepertoire similar to the adult of the species, the motorbehaviors of the altricial newborn rat pup are relativelylimited (Altman & Sudarshan, 1975; Bolles & Woods,1964; Eilam & Golani, 1988). Newborn rat pups areconfined to the nest for most of the early postnatalperiod and express only a few basic motor patterns.Nipple attachment and righting are examples of twosuch patterns. The pup must gain access to the nipple

Correspondence to: W. P. SmothermanContract grant sponsor: NICHHDContract grant number: HD 16102

to suckle and survive. The purpose of the present studywas to describe patterns of motor behavior in the1-day-old rat pup important for gaining access and at-taching to the nipple.

Several studies have described the motor repertoireof the newborn rat pup, characterizing it as relativelysimple and stereotyped and suggesting that some earlymotor movements are precursors of more advanced(adult) behavior (Coghill, 1929; Eilam & Golani,1988; Golani & Fentress, 1985). In the course of on-togeny, a more-diverse motor repertoire is achievedwhen new types of movements are incorporated intoexisting patterns of behavior. Expansion of the motor

58 Eilam and Smotherman


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repertoire is accompanied by changes in the centraland peripheral nervous systems (Cabana, Jolicoeur, &Baron, 1990; Viala, Viala, & Fayein, 1980), muscu-lature (Oron, 1990), and morphology (Peters, 1983).Consequently, it has been suggested that behaviorswhich appear different in structure and function in theadult animal may have shared common motor ante-cedents earlier in their ontogeny (Carrier, 1996; Eilam& Golani, 1988). In order to assess the validity of thishypothesis, the present study provides a detailed de-scription of the kinematic structure of movements in-volved in the newborn rat’s achieving a supine postureunder the mother so that the pup can gain access to anipple. The description of the pup’s movement to asuckling posture is compared to descriptions of right-ing behavior, pivoting locomotion, and quadrulateralstepping in the neonatal rat pup. It is proposed thatthese basic patterns of motor behavior expressed earlyin development share common, reminiscent motorstructures.

METHODS

Subjects

Subjects were twenty 1-day-old rat pups from 10 lit-ters. Pups were produced by time-mating adultSprague-Dawley rats (Charles River Laboratories,Wilmington, MA) in the Laboratory of Perinatal Neu-roethology at Binghamton University. Adult rats werehoused in groups of 3 females and 1 male in plasticbreeding cages Vaginal smears(36 3 47 3 20 cm).were collected daily during a 4-day breeding period.After removal of the breeding male, pregnant rats weremaintained under conditions of constant room tem-perature (227C), on a 12 : 12 hr light : dark cycle (lightson at 0700/hr) until birth of the litter (Day 0). Litterswere culled to 10 pups on the day of birth. Food andwater were available ad libitum to adult rats. At alltimes, rats were maintained and treated in accordancewith guidelines for animal care and use established bythe National Institutes of Health (1986).

Apparatus

A transparent Plexiglas observation box (30 3 15 3was used for all behavioral observations. The15 cm)

box had holes ( diameter) on two sides to permit8 mmair to enter. A mirror was positioned under the floorof the box and tilted at a 45-degree angle to provide abottom view of the mother and experimental subjectsand to permit unobstructed videotaping of mothers andpups during all test sessions. A light blue fabric was

located on the top of the box and served as a high-contrast background for the videotaping of the femalerat and test subject. The transparent observation boxwas illuminated by a 500-W halogen light positionedon the floor of the testing room. A video camera (Pan-asonic Pro-line model AG-456) was placed in front ofthe mirror at a distance of for videotaping the1.5 mbehavior of test pups. The temperature of the test ap-paratus was held constant at 227C.

Testing Procedure

The mother and litter were removed from the animalcolony and taken to the laboratory before the start5 hrof behavioral testing. Pilot data indicated that pupswould attach rapidly after a 5-hr separation. Five pupswere separated from the mother and placed togetherin a box in an incubator that was(15 3 15 3 5 cm)maintained at a temperature of 307C. The mother and5 additional pups were left undisturbed in the homecage. Before testing, mother and pups were removedfrom the home cage and placed in the observation boxfor a 30-min adaptation period. The mother remainedin the observation box after the adaptation period andthe pups were removed and returned to the home cage.One test pup was taken from the incubator and placedin the observation box, in a prone position, facing themother, with the tip of its nose at a distance of 2 cmfrom the side of the mother. No attempt was made tostandardize the behavior of the mother at the time pupswere introduced into the test chamber. The behaviorof the test pup was videotaped continuously for 10min. Whenever the pup exhibited an oral grasp re-sponse, it was removed from the nipple and permittedto approach the female again. Individual test pups ex-hibited a mean of oral grasp responses. Af-5.6 6 3.2ter the 10-min session, a 2nd test pup from the litterwas tested under the same conditions. All observationswere conducted between 1300 and 1700 hr.

Behavior Analysis and Statistics

The motor behavior of the test pup was scored duringreduced-speed playback of the videotape record.Whenever an oral grasp response was observed, thepreceding behavior was noted, as was the posture ofthe pup. For this notation, the pup’s trunk was consid-ered to have three articulated segments: head, chest,and trunk (see Eilam & Golani, 1988). Movements ofthese three articulated trunk segments were scored asfollows: (a) Rotation involved a turning of the segmentalong its longitudinal axis; (b) ventroflexion involveda moving of the chest and pelvis to achieve a U-shapedposture; (c) dorsiflexion involved a straightening of

Approach to the Nipple 59


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the chest and pelvis and resulted in an uncurling of thetrunk from the U-shaped posture; (d) lateral steppingof the forelegs was scored whenever the head movedlaterally and was then placed on one foreleg while theother foreleg stepped sideways, to lay flexed along theside of the head. Ultimately, the foreleg which wasunder the head stepped sideways so that it was pulledfrom underneath the head and placed along the side ofthe head; (e) crawling involved sequential stepping ofall four legs (Stepping was not scored for each legseparately.) which resulted in forward transportationof the trunk was scored as crawling. The sequence ofstepping then was further classified into a lateral step-ping sequence (HL, FL, HR, FR), a diagonal steppingsequence (HL, FR, HR, FL), or a different steppingsequence; and (f) posture in relation to gravity wasscored for each segment, by indicating which side ofthe segment was in contact with the floor of the box(e.g., dorsal, ventral, lateral-right, or lateral-left). Eachof the above movements, together with the time oftheir initiation, was recorded to provide the sequenceof movements performed by the test pup while it ap-proached and gained access to the nipple. Other actsincluding the oral grasp of the nipple or suckling werenoted whenever they occurred. Nonparametric chi-square tests of independence were used to compare theincidence of the different categories of movement.

RESULTS

Final Posture of the Pup at Timeof Oral Grasp Response

There were 106 instances where the test pup graspeda nipple. In 102 of these 106 cases (96.2%) the pupwas in a supine posture, either partially or completelyunder the ventral surface of the mother when the oralgrasp response was performed. In three cases, the pupwas on its side when oral grasping occurred, and inone case, the pup grasped the nipple while in a proneposture under the mother (Table 1). Test pups were ina supine posture significantly more often when per-forming an oral grasp response, x2, (df 5 2) 5

Therefore, the 1-day-old pup typi-283.1, p , .001.cally assumes a supine posture under the mother be-fore grasping a nipple to initiate suckling.

Approach to the Mother’s Ventral Surface

In 86 of the 106 cases (81%) where the test pupgrasped a nipple, the pup crawled to the mother. Alateral stepping sequence (e.g., HL, FL, HR, FR) wasobserved in 40 cases of forward crawling to the

mother. In this lateral sequence, a step of a hindlegwas followed by a step of the ipsilateral foreleg, andthe step of the foreleg was followed by a step of thecontralateral hindleg. In seven cases, crawling in-cluded a diagonal stepping sequence (e.g., HL, FR,HR, FL). In both lateral and diagonal sequences, a stepof a foreleg was followed by a step of a hindleg andvice versa. Six other cases involved a successive step-ping sequence where movement of the forelegs wasfollowed by movement of the hindlegs (e.g., HL, HR,FL, FR). Thirty-three other instances of stepping dur-ing approach to the mother were not scored becausethey did not include at least one step of each leg, orbecause the leg(s) were not observable (Table 1). Acomparison of the different patterns of approach to themother indicated that lateral stepping sequence wasmost prevalent as pups approached the mother, x2,(df 5 2) 5 74.7, p , .001.

In 20 of the 106 cases (19%) the test pup graspeda nipple after being picked up by the mother (Table1). In these cases, the mother held the pup and engagedin anogenital licking. The pup’s head was closed tothe thoracic-most pair of the mother’s nipples and afteranogenital licking, and in some cases during the boutof anogenital licking, the pup grasped a nipple.

Position of Pup at Time ofOral Grasp Response

Different parts of the pup’s body were in contact withthe ventral surface of the mother when oral graspingoccurred. In 72 of the 106 cases (67.9%), the pup’sentire trunk was in contact with the ventral surfacewhen the oral grasp response occurred. In another 25cases (23.6%), only the pup’s head and chest wereunder the mother and in 9 cases (8.5%) pups graspedthe nipple when only the head or snout was under themother’s trunk (Table 1). The oral grasp response wasseen most often when the pup’s body was completelyunder the mother, x2, (df 5 2) 5 91.0, p , .001.

Mother’s Behavior Altersthe Supination Process

In 65 cases (61.3%), the dam crouched, permitting thetest pup access to her ventral surface and nipples (Ta-ble 1). The mother’s behavior altered the supinationprocess in 41 cases (38.7%) where the pup eventuallygrasped a nipple (Table 1). The dam could interveneat any phase of the process. In 20 of these cases ofintervention, mother’s movement rolled the pup to asupine posture after which it grasped a nipple. In 21of these cases, the dam picked up the pup and engagedin whole body or anogenital licking with the pup in a



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Table 1. Movements of the Pup During Supination

Behavior Category/Structure Subcategory

1. Final posture of pup at the time oforal grasp response

SupineLateralProne

10231

2. Approach to the mother’s ventralsurface

Crawled to mother 86 Lateral step 40Diagonal step 7Successive step 3Not observable 36

Placed by mother 20

3. Position of pup at time of oral graspresponse

Pup entirely under the motherPup’s head and chest under mother

7225

Pup’s head or snout under mother 9

4. Mother’s behavior alters supinationprocess

None (just crouching)Mother’s movement rolled pup to supineMother picked up pup

652120

5. The kinematic structure of move-ments as the pup supinates

Phases I 1 II 1 III, (no intervention)Phases I 1 II, then mother intervenedPhase I, then mother intervenedMother intervened before Phase IGrasp, then rotate to supine posture

575

1620

8

6. Foreleg stepping on the maternalventral surface by pups in a supineposture

Sideways stepping during Phase INo sideways stepping in Phase I

7432 Mother intervened 31

Grasp while prone 1Sideways stepping during Phase IIINo sideways stepping in Phase III

5818 Mother intervened 18

7. Activity around the nipple while in asupine posture

Pup supinated, stepped on mother’s ven-tral surface, then exhibited oral graspresponse

94 Lateral sequence 33Other sequences 5Not observable 56

Pup exhibited oral grasp response, thensupinated

12

supine posture. In some of these cases, the pup graspeda nipple either during the bout of licking or after itstermination.

Kinematic Structure of Movementsas the Pup Supinates

Frame-by-frame analysis of the videotape records wascompleted to examine the motor movements per-formed as the pup turned from a prone to a supineposture. This analysis revealed that the supine posturewas achieved by a sequence of motor behaviors thatwere carried out in a typical order. Starting from aprone posture (Figure 1a), the pup stretched forwardand rotated its head along the longitudinal axis. Duringthis rotation, the head was lifted up in relation to thetrunk. Rotation of the head continued after the headwas lifted whether the pup was close to a nipple or not(Figure 1b). Rotation of the forequarters (forelegs and

chest) followed, resulting in a twisting of the trunkwhile the side of the head and forequarters were onthe floor of the test box. The hindquarters remained ina prone position during this rotation (Figure 1c). Thehindquarters then were recruited to accompany the ro-tation, and the pup completed a partial turn to achievea posture where the lateral side of the trunk was incontact with the floor of the test box. Once attainingthis posture, the pup executed a ventroflexion of thetrunk, so that the head and the pelvis were broughtclose to each other in a U-shaped posture. This posturewas accomplished while the pup lay on its side (Figure1d). Next, the pup executed a rapid dorsiflexion mov-ing its trunk from the U-shaped posture (Figure 1e).At the peak of this movement, the pup rotated its head,and then rotated the forequarters (Figure 1f). Ulti-mately, the hindquarters were rotated. These move-ments resulted in the pup’s entire trunk attaining asupine posture (Figure 1g).



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FIGURE 1 Starting from a prone posture (a), the pup stretches forward and rotates its head alongthe longitudinal axis, and the head is lifted up in relation to the trunk. Rotation of the head continueswhether the pup is close to a nipple or not (b). Rotation of the forelegs and chest follows, resultingin a twisting of the trunk while the side of the head and forequarters remain in contact with thesurface of the test chamber. The hindquarters remain in a prone position during this rotation (c). Thehindquarters then are recruited into the movement, as the pup completes a partial turn to achieve aposture where its side is in contact with the substrate. While on its side, the pup executes a ventro-flexion of the trunk, so that the head and the pelvis are brought close to each other in a U-shapedposture (d). Ventroflexion is followed by a rapid dorsiflexion as the trunk moves from the U-shapedposture (e). At the peak of the dorsiflexion, the pup rotates its head and forequarters (f). Finally, thehindquarters are rotated as the pup attains a supine posture (g).

Movements of the pup as it achieved a supine pos-ture could be divided into three phases. The first phaseinvolved cephalocaudal rotation after which the puplay on its side (Figure 1a, 1b, 1c). The second phaseinvolved ventroflexion where the trunk was arched sothat the pup achieved a U-shaped posture, and a sub-sequent dorsiflexion of the trunk (Figure 1d, 1e). Thethird phase involved a cephalocaudal rotation wherethe pup moved to a supine posture (Figure 1f, 1g). In57 of the 106 cases (53.7%), the pup exhibited all threephases to achieve a supine posture. In another 21 cases(19.8%), these phases were interrupted when themother intervened to rotate or place the pup under herventral surface. In 20 cases (18.9%), the mother inter-vened before the pup exhibited any of the phases. In8 cases (7.5%), the pup grasped a nipple and then ro-tated to the supine posture after the oral grasp.

Foreleg Stepping on Maternal VentralSurface by Pups in a Supine Posture

After achieving a supine posture under the mother,some pups exhibited stepping movements with theforelegs. These foreleg movements often resembled“punting” (Altman & Sudarshan, 1975). The head wasrotated and placed over one of the forelegs while the

other foreleg extended laterally (Figure 1b). The chestwas then rotated (Figure 1c) which involved steppingwith the forelegs. The foreleg under the head wasmoved sideways, on the mother’s ventral surface. Theother foreleg also stepped sideways during the chestrotation, so that the pup was positioned on its side. Asimilar pattern of stepping with the forelegs was evi-dent in the third phase of the supination process (Fig-ure 1f, 1g). This stepping pattern was observed when-ever the mother did not intervene (Table 1). Duringthe cephalocaudal rotations in the first and secondphases, the hindlegs displayed forward-steppingmovements. Typically, these were “air stepping”movements (Van Hartesveldt, Sickles, Porter, & Ste-houwer, 1991) because the hindpaws did not contacteither the surface of the test box or the mother’s ventralsurface. This sequence of punting and stepping move-ments was evident in the first phase in 74 cases(69.8%) and in the third phase in 58 cases (54.7%).

Activity Around the Nipple Whilein a Supine Posture

Once establishing contact with the mother, the test pupwould supinate and then exhibit stepping movementsto bring it to the area surrounding one of the mother’s



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nipples. The pup then would engage in scanningmovements (Blass & Teicher, 1980), until it exhibitedan grasp response (Smotherman, Goffman, Petrov, &Varlinskaya, 1997). These stepping, scanning, andgrasping behaviors also were evident when the motherheld the pup under her ventral surface. The pup ex-hibited stepping movements on the maternal ventralsurface while in the supine posture in 94 cases(88.7%). In another 12 cases (11.3%), the pup graspeda nipple without any stepping movements.

The simultaneous view of all four limbs was notalways possible when pups engaged in stepping move-ments while in a supine posture under the mother.Such a view was necessary for scoring the steppingsequence. Lateral stepping (e.g., HL, FL, HR, FR) wasobserved in 33 of the 94 cases where some steppingoccurred (35.1%). Diagonal and gallop sequenceswere observed in only 5 cases (5.3%). In the remaining56 cases, at least one of the legs was hidden, or thepup switched the stepping sequences before complet-ing a cycle including at least one step with each leg,and therefore it was not possible to identify the step-ping sequence.

DISCUSSION

Significance of the Supine Posturefor Oral Grasping of the Nipple

In order to afford the newborn rat pup access to thenipple area and to provide a relatively warm and pro-tected environment, the mother exhibits a kyposis pos-ture (Stern, 1996). During kyposis, the back is archedover the fore- and hindlegs, such that the ventral sur-face is elevated (Stern & Johnson, 1990). With themother in this posture, the pup can move into the spacecreated, engage in nipple search behavior, grasp a nip-ple, initiate suckling behavior, and ingest milk (Stern& Lonstein, 1996). In the present experiment, detailedframe-by-frame analyses of videotape records from 1-day-old pups during approach to and oral grasping ofa nipple indicate that rotations to adopt a supine pos-ture: (a) are initiated after the pup crawls underneaththe mother, (b) occur regardless of nipple location, (c)typically precede nipple search behavior, and (d) arecomprised of three identifiable phases including ce-phalocaudal rotation, ventroflexion, and a second ce-phalocaudal rotation.

Suckling in the older (e.g., 10-day-old) rat pup iscomprised of a number of discrete motor events, eachwith their control mechanisms (Hall, 1990). First, thepup moves toward the mother, which can involve ac-tive stepping movements of the forelimbs and the rear-

limbs. Contact with fur on the mother’s ventral surfacestimulates scanning and probing movements with thehead. When the nipple is encountered, the pup exhibitsmouthing and licking movements that culminate inoral capture, grasping, and attachment to a nipple(Blass & Teicher, 1980). Access to a nipple by the1-day-old pup involves more motor events. The 1-day-old pup engages in a lateral stepping sequence duringapproach to the mother. After making contact with themother’s ventral surface, there is a cephalocaudal ro-tation of the head and trunk. The pup then exhibitsventroflexion of the trunk to achieve a U-shaped pos-ture, which is followed by a subsequent dorsiflexionfrom the U-shaped posture. Next there is a secondcephalocaudal rotation moving the pup to a supineposture. In this supine posture the pup “locomotes” onthe maternal ventral surface in a punting-like fashion.While in a supine posture, the pup searches for a nipplewith scanning and probing movements with the head.Finally, perioral contact with the nipple results in oralgrasping of the nipple and the process culminates innipple attachment. This sequence of behaviors is per-formed by the newborn rat pup within a few hours ofdelivery, and without any assistance from the mother.

Oral Grasping of the Nipple inthe Supine Posture May InvolveActive Suppression of Righting

One of the early motor patterns expressed by the de-veloping rat pup is righting (Pellis, Pellis, & Teitel-baum, 1991). When the pup finds itself in a supineposture, it normally will exhibit righting behavior toreestablish the prone posture which is preferred. Right-ing behavior has been observed in the rat pup on theday of birth (Pellis et al., 1991). To achieve a supineposture, which the pup adopts to grasp a nipple, thepup must adjust its posture away from a prone posture.This raises a question as to whether movement to thesupine posture that permits oral grasping of a nippleinvolves an active suppression of righting behavior.Indeed, when the newborn rat pup in a supine postureis stimulated with an artificial nipple, it does not ex-hibit righting behavior but remains in the supine pos-ture and expresses mouthing, licking, and oral grasp-ing of the artificial nipple (Smotherman et al., 1997).These observations suggest that gentle tactile stimu-lation of the perioral region results in a suppression ofrighting behavior.

Righting behavior has been suppressed in youngand adult rats by a procedure where the head and neckare bandaged (De-La-Cruz, Junquera, & Russek,1987). In this study, the authors note that the postureof the bandaged rat pup is “very similar to a posture



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FIGURE 3 Stepping movements involved as pups supi-nate (from present experiment) and right (adapted from Pel-lis et al., 1991).

FIGURE 2 Head, trunk, and leg movements involved aspups supinate (from present experiment) and right (adaptedfrom Pellis et al., 1991).

the pup adopts while suckling from the mother.” De-La-Cruz and colleagues (1987) hypothesized that dur-ing normal nursing behavior, the mother’s weight mayexert pressure on the pup and elicit dorsiflexion of thehead and upper torso, as seen in bandaged pups. In-deed, dorsiflexion is one component of the sequencewhereby pups in contact with the mother rotate toachieve a supine posture (Figure 1). Stimulation of theperioral region of the newborn rat pup with a brushmade from the lactating female’s ventral fur (NorikoKodama, unpublished observations), as well as peri-oral stimulation with a soft surrogate nipple (Smoth-erman et al., 1997), are effective in suppressing right-ing.

Similarities in the Kinematic Structureof Supinating and Righting

Rotation to the supine posture is markedly similar torighting in that it involves the same motor compo-nents. The findings of the present study suggest thatrighting behavior and rotation to the supine posturewhile in contact with the mother’s ventral area can becharacterized as having a similar kinematic structure,with one difference that righting is performed with theforce of gravity and movement to the supine postureis performed against the force of gravity (Figure 2).

While trunk movements performed as the pup su-pinates are reminiscent of trunk movements performedduring righting, the stepping movements performeddiffer between the two behaviors (Figure 3). Yet thestepping sequence during righting resembles the step-

ping sequence exhibited during punting, another formof quadrupedal locomotor activity (Altman & Sudar-shan, 1975; Robinson & Smotherman, 1992a, 1992b).In punting, the pup pivots around its hindquarterswhile the head acts as a “fifth limb.” During this formof locomotion, the head is moved laterally over one ofthe forelegs as the snout establishes contact with thesubstrate. The pup then transfers weight to the snout,thus unloading weight from the leg. After the weighttransfer, the leg is moved to the side of the head. Lat-eral movements of the head and chest result in a lateralextension of opposite foreleg. From this extended pos-ture the leg steps to the side of the head (Altman &Sudarshan, 1975; Robinson & Smotherman, 1992a,1992b). The punting movement culminates when thehindlegs slide or step and adjust the pelvis to a newposition. The motor sequence involved in punting, thatincludes head movement, alternate sideways steppingof the forelegs, and adjustment of the pelvis to a newposition relative to the head and chest, is similar to thesequence seen as 1-day-old rat pups supinate to graspa nipple.

Motor Modules in the Expression ofBehavior by the Newborn Rat Pup

Studies of the ontogeny of motor behavior have sug-gested the existence of motor components or buildingblocks from which more complex patterns of move-ment are formed. These include lateral movements ofthe head, vertical movements of the head and steppingmovements (Bekoff, 1981; Coghill, 1929; Eilam &Golani, 1988). Other studies have identified more in-



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Table 2. Early Motor Patterns That Result From Interactions Between a Limited Set of Motor Modules

Bodywise movements

Ventroflex Dorsiflex Rotation

Absolute movements

Lateral Forward Vertical

Stepping

Forelegs Hindlegs

Righting 1 1 1Supinating 1 1 1 SidewaysPunting 1 Sideways BackwardPivoting 1 Sideways ForwardWalk 1 Forward ForwardRearing 1Climbing 1 Forward

tegrated motor behaviors such as punting, pivoting,walking, running, rearing, and climbing (Altman &Sudarshan, 1975; Blumberg-Feldman & Eilam, 1994;Bolles & Woods, 1964; Fentress, 1992; Pellis et al.,1991) that derive from an assemblage of these com-ponents. However, in a recent study, Pellis (1996) pro-posed that there is an intermediate level of organiza-tion between the motor component and finalexpression of the motor movement pattern. Pellis(1996) proposed the term motor module for such anintermediate level of organization. Moreover, in ana-lyzing righting behavior in rats and marsupials, Pellis(1996) suggested that there are separate motor mod-ules for the trunk and for the limbs that are integratedand result in the expression of different motor patterns.The results of the present experiment suggest thatmoving to the supine posture results from a combi-nation of different modules present in the motor rep-ertoire of the fetal rat (Altman & Sudarshan, 1975;Bolles and Woods, 1964; Robinson & Smotherman,1992a, 1992b; Stern, 1996). Further, these preexistingmotor modules appear to be the basis for other typicalmotor behaviors expressed by the newborn rat. Forexample, ventroflexion already is evident in the ratbefore birth. Rat fetuses exhibit ventroflexion re-sponses in the uterus between Days E17 and E21(Smotherman & Robinson, 1988). Similarly, dorsi-flexion is important for the expression of righting be-havior shown by the rat pup on the day of birth (Pelliset al., 1991). Ventroflexion is involved during the ex-pression of righting as well as when the pup rotates toa supine posture before nursing.

Cephalocaudal incorporation of trunk segmentsinto movement has been proposed as an underlyingprocess during the recovery of motor behavior afterlesion to the nigro–striatal pathway (Golani, Wolgin,& Teitelbaum, 1979), in the postnatal ontogeny of ex-ploratory behavior (Eilam & Golani, 1988; Golani,1992), and in the ontogeny of vertebrate locomotion(Eilam, 1995). However, the above-mentioned studieshave concentrated on describing cephalocaudal rota-tions in the lateral, forward, and vertical spatial di-

mensions of movement (absolute system of referencefor these movements). Results from the present ex-periment, together with the results from studies ofrighting behavior (Pellis et al., 1991) add rotationalong the body axis as another dimension of move-ment in which cephalocaudal activity is apparent(bodywise system of reference for this movement).Cephalocaudal rotation is a basic motor module and acomponent of several types of righting (Pellis, Pellis,& Nelson, 1992; Pellis et al., 1991).

Lateral stepping involves alternate stepping in eachgirdle and between different girdles (Blumberg-Feld-man & Eilam, 1994; Collins & Stuart, 1994). This typeof stepping is the initial form of forward quadrupedalstepping seen during postnatal development in variousrodent species. Lateral stepping has been observed inthe rat fetus (Bekoff & Trainer, 1979; Robinson &Smotherman, 1992a, 1992b), is considered an ances-tral and stable gait in tetrapods (Dagg, 1973), and isoriginally linked to the lateral movements of the trunk(Coghill, 1929).

In Table 2, we depict different motor patterns per-formed by rat pups which result from interactions be-tween a limited set of motor modules. It is proposedthat the rat pup achieves a supine posture under themother to access the nipple for suckling through in-teractions between a preexisting and limited set of mo-tor modules. These modules are not unique to expres-sion of this early behavior but are involved in theconstruction of much of the motor behavior of thenewborn rat pup and perhaps the rat fetus as well(Robinson & Smotherman, 1992a, 1992b).

CONCLUSIONS

The present study provides a detailed description ofone important early behavior and characterizes howthe newborn rat pup moves from a prone posture awayfrom the mother to a supine posture under the motherin order to gain access to a nipple. Expression of thismotor behavior is vital for the survival of the newborn



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rat. It is proposed that the pup achieves a supine pos-ture under the mother through the recruitment of motormodules, which are reminiscent of the trunk move-ments expressed during righting as the pup movesfrom a supine to a prone posture. The stepping se-quence expressed by the pup while in the supineposture under the mother resembles the stepping ex-pressed during punting, a basic, quadrupedal, loco-motor activity shown by the newborn rat pup (Altman& Sudarshan, 1975). On the basis of these structuralsimilarities, we proposed that basic motor modules(Pellis, 1996) are being combined in different waysand result in expression of an expanded repertoire ofmotor behaviors early in development. Other investi-gators have commented on the existence of commonmotor modules during early ontogeny and suggestedthat they should be considered as an ancestral basis fordiversification of motor activity in later phases in on-togeny (Eilam & Golani, 1988; Golani, 1992; Robin-son & Smotherman, 1992a, 1992b). The manifestationof these motor modules in different species which areremote in a phylogenetic sense (Pellis et al., 1992)lends support to the notion that the modules are offundamental importance during early mammalian de-velopment.

Motor performance in pups is the product of aninteraction between neural control mechanisms anddevelopmental changes in musculature, support, andother body systems (Cabana et al., 1990; Oron, 1990;Peters, 1983; Viala et al., 1980). These systems areimmature in the newborn rat pup, resulting in a limitedcapacity for function. The application of a basic set ofmotor modules to permit expression of different be-havioral functions in early ontogeny provides a par-simonious and relatively simple structure for the elab-oration of behavior which meets the limited capacityof other developing systems.

NOTES

Dr. David Eilam was a Visiting Scientist at the Center forDevelopmental Psychobiology at Binghamton University—SUNY.

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Documents

How the neonatal rat gets to the nipple: Common motor modules and their involvement in the expression of early motor behavior