Applied Animal Behaviour Science 100 (2006) 48–57

www.elsevier.com/locate/applanim

Onset of sentience: The potential for suffering

in fetal and newborn farm animals§
David J. Mellor *, Tamara J. Diesch
Animal Welfare Science and Bioethics Centre, Massey University,
Palmerston North, New Zealand

Available online 12 May 2006

Abstract
Sentience and consciousness are prerequisites of suffering. Thus, animals must have sufficiently
sophisticated neural mechanisms to receive sensory information and to transduce this information into
sensations, and they must also be conscious to be able to perceive those sensations. Moreover, those
sensations must be sufficiently noxious or aversive to cause suffering. The neural apparatus of embryos and
fetuses of farm animals is inadequate to support sentience for at least the first half of pregnancy, but the
required structures and mechanisms do develop by the time of birth. Thus, although one of the preconditions
for suffering is satisfied shortly before birth, the embryo and fetus are apparently never conscious for the
following reasons. The embryo-fetus initially does not have brain structures that are functionally capable of
supporting consciousness, and subsequently, when the fetal brain might have that capability, it displays
electrical activity indicating a continuous state of sleep and therefore unconsciousness. Furthermore, the
fetus is apparently actively maintained in sleep-like states by several endogenous neuroinhibitory
mechanisms which involve adenosine (a potent neuroinhibitory and sleep inducing agent), allopregnanolone
and pregnanolone (two neurosteroidal anaesthetics), prostaglandin D2 (a potent sleep-inducing hormone), a
placental neural inhibitor, warmth, buoyancy and cushioned tactile stimulation. Consciousness evidently
appears for the first time only after birth. This results from a substantial withdrawal of the neuroinhibitors,
especially adenosine, and the involvement of neuroactivators including 17b-oestradiol (a potent neuroactive
steroid with widespread excitatory effects in the brain), noradrenaline (released from excitatory locus
coeruleus nerves that extend throughout the brain), and a barrage of novel sensory information associated
with the newborn’s first exposure to air, gravity, hard surfaces, unlimited space and, usually, to cold ambient
conditions. We conclude that the embryo and fetus cannot suffer before or during birth. Furthermore, we
conclude that suffering can only occur in the newborn when the onset of breathing oxygenates its tissues
sufficiently to substantially reduce the dominant adenosine inhibition of brain electrical activity.

§
This paper is part of the special issue entitled Sentience in Animals, Guest Edited by Dr John Webster.
* Corresponding author. Tel.: +64 6 350 4807/356 9099; fax: +64 6 350 5657.
E-mail address: D.J.Mellor@massey.ac.nz (D.J. Mellor).

0168-1591/$ – see front matter # 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2006.04.012
 D.J. Mellor, T.J. Diesch / Applied Animal Behaviour Science 100 (2006) 48–57 49

The implications of these observations for managing fetuses and newborns in ways that minimise suffering
are considered briefly.
# 2006 Elsevier B.V. All rights reserved.

Keywords: Fetus; Birth; Newborn; Neural development; Neuroinhibitors; Neuroactivators; Unconsciousness; Suffering

1. Introduction

An animal must be both sentient and conscious for suffering to occur. The first prerequisite,
therefore, is that the required neural apparatus for sentience must be in place and operational.
Internal and environmental stimuli must be able to elicit impulse transmission along nerves from
sensory receptors to the animal’s brain, and its brain stuctures must be operationally sophisticated
enough to transduce those nerve impulses into perceived sensations. The second requirement is
that the brain must be in a functional state that allows the animal to perceive sensations; it must be
in a state that supports consciousness, as unconsciousness nullifies perception. Third, for a
conscious animal to suffer, and for its welfare thereby to be compromised, the character, intensity
and/or duration of the sensations it perceives must result in significantly noxious or aversive
experiences (Mellor and Reid, 1994; Mellor and Stafford, 2001).
Although it is not clear whether there is a distinct place delineating those animals in the
phylogenetic hierarchy that are and are not sentient or whether sentience exhibits different levels
(Mellor, 1998; Kirkwood, 2006), it is generally accepted that mammals are sentient. However,
this generalisation requires some qualification because it does not allow for different phases of
development. Adult and autonomous young mammals are evidently sentient, as are
neurologically mature young very soon after birth (Mellor and Gregory, 2003; Mellor and
Stafford, 2004), but the situation in neurologically immature newborns and in mammalian young
before birth is less obvious.
The present paper explores the potential of fetuses and newborns to suffer by outlining the
development of the neural apparatus required to support sentience and the functional state of that
apparatus with respect to consciousness before and after birth. State changes at birth and the
impact of other factors on the potential for suffering after birth are also considered. Although
most reported observations relate to fetal and newborn sheep, the principles are considered to be
generally applicable to farmed ungulates (e.g. sheep, goats, cattle, deer, horses and pigs).

2. Prenatal development of the neural apparatus required for sentience

Neural tissue begins to differentiate after fertilisation, progressing via sparsely connected
rudimentary precursors of nerve tracts and brain structures in the embryo to the well-defined,
complex, sophisticated and operationally effective, yet still maturing, structures that are present
in the fetus just before birth (Mellor and Gregory, 2003). As part of this development, sensory and
numerous other neurological structures need to mature sufficiently in utero to enable the newborn
to use sight, hearing, smell, taste, touch, proprioception and thermal sensitivity to secure its
survival during the critical first few minutes and hours after birth (Mellor and Gregory, 2003;
Mellor and Stafford, 2004). The operation of such sensory perception very soon after birth shows
that the required structures are in place immediately before birth, and possibly earlier. Fetal sense
organs therefore have the potential to operate in utero. The question is, do they? In fact, the
sensory environment in utero is significant and varied, and the fetus in late pregnancy is
50 D.J. Mellor, T.J. Diesch / Applied Animal Behaviour Science 100 (2006) 48–57

responsive to stimulation in most of the modalities evident after birth (Bradley and Mistretta,
1975; Abrams et al., 1996; Bauer et al., 1997). Thus, fetal sense organs do operate, but this does
not mean that the fetus perceives the associated sensory input. For that to occur, a fetal neural
state that supports consciousness would need to be present.

3. Functional state of the neural apparatus in the fetus

The nervous system is evidently too immature to support any activity resembling
consciousness during the embryonic stage of development and this immaturity apparently
continues at least into the early fetal stage (Joseph, 2000). Indeed, the establishment of the
necessary neural pathways and their connections to lower brain centres and then to the cerebral
cortex, together with the evolution of mature fetal brain electrical activity (described briefly
below) and cortical responses to somatic tactile stimulation (Bradley and Mistretta, 1975;
Fitzgerald, 1999; Joseph, 2000; Mellor and Gregory, 2003), suggest that, even if the
physiological environment of the brain permitted it, neural development could not support fetal
consciousness until later in pregnancy.
The electrical activity of the fetal cerebral cortex (EEG activity) provides apparently definitive
evidence of the absence of consciousness in utero. Thus, from mid-pregnancy fetal EEG activity
evolves from rudimentary and discontinuous patterns into two coherent, discrete states
resembling rapid-eye-movement sleep and non-rapid-eye-movement sleep in postnatal animals
(Harding et al., 1981; Clewlow et al., 1983; Szeto and Hinman, 1985; Berger et al., 1986; Dawes,
1988). By late pregnancy these two sleep-like states occupy 95% of fetal EEG activity during
each day, the other 5% representing transitions between the two sleep-like states (Mellor et al.,
2005). Accordingly, in considering the whole of pregnancy, the embryo-fetus initially does not
have brain structures which are functionally capable of supporting consciousness, and
subsequently, when the brain might have that capability, the fetus displays EEG activity
indicating that it is continuously asleep and therefore unconscious.

4. Maintenance of fetal sleep-like states

The above conclusion is further strengthened by an increasing body of evidence which shows
that there are several suppressors in utero that act to inhibit neural activity in the fetus. Thus, the
uterus plays a key role in providing the chemical and physical factors that together help to keep
the fetus continuously asleep. We propose that this is achieved, among other things, through the
combined neuroinhibitory actions of a powerful EEG suppressor and sleep inducing agent
(adenosine), two neurosteroidal anaesthetics (allopregnanolone, pregnanolone) and a potent
sleep-inducing hormone (prostaglandin D2), acting together with a possible peptide inhibitor
produced by the placenta, further supported by the warmth, buoyancy and cushioned tactile
stimulation of the uterine environment (Mellor and Gregory, 2003; Mellor et al., 2005).
Adenosine is a potent neural inhibitor which promotes sleep and/or unconsciousness and is
produced by placental and fetal tissues in quantities that maintain its circulating concentrations
two- to four-fold higher in the fetus than in the mother (Ball et al., 1995, 1996; Dunwiddie and
Masino, 2001). Superimposed on these high background concentrations are variations due to
changes in fetal oxygen status, such that hypoxaemia (oxygen shortage) elevates and
hyperoxaemia (experimentally induced oxygen abundance) reduces adenosine concentrations,
which in turn lead, respectively, to suppressive and activating effects on fetal EEG, breathing
movements and behavioural activities (Szeto and Hinman, 1985; Szeto and Umans, 1985; Koos
 D.J. Mellor, T.J. Diesch / Applied Animal Behaviour Science 100 (2006) 48–57 51

and Matsuda, 1990; Sawa et al., 1991; Avital et al., 1993; Kubonoya and Power, 1997; Koos et al.,
2001). Changes in adenosine effects can occur very rapidly in view of its exceptionally short
biological half-life of 0.6–1.5 s (Moser et al., 1989).
Allopregnanolone and pregnanolone are neuroactive steroids with well-established
anaesthetic, sedative/hypnotic and analgesic effects (Majewska, 1992; Paul and Purdy, 1992;
Miller, 1998). They are produced from cholesterol or progesterone by the placenta and the fetal
brain, exhibit high circulating concentrations in the fetus and have suppressive effects on fetal
EEG, eye movements, breathing movements and postural changes (Crossley et al., 1997; Nicol
et al., 1997, 1998, 1999, 2001; Hirst et al., 2000).
Prostaglandin D2, a potent sleep-inducing agent in adult mammals (Hayaishi and Urade,
2002), is evidently active as a suppressor of eye, breathing and postural muscle movements, and
associated EEG activity, in the late gestation fetus (Lee et al., 2002).
Likewise, a possible placental peptide inhibitor, warmth, cushioned tactile stimulation and
buoyancy are also considered to contribute to the maintenance of sleep-like EEG activity in the
fetus until birth (Mellor and Gregory, 2003).
It appears, therefore, that the above factors, and others (Mellor et al., 2005), contribute to
actively maintaining the continuous sleep-like state of the fetus (indicated by its EEG)
throughout the last one-third to one-half of pregnancy.

5. Changes in the functional state of the brain at birth

5.1. Suppressors of brain function and their removal

As labour approaches there is a progression towards fetal EEG activity indicating a

predominance of deeper sleep-like states (Berger et al., 1986; Shinozuka and Nathanielsz, 1998),
and during labour fetal motor systems, including the respiratory system, are largely quiescent
(Berger et al., 1986; Fraser and Broom, 1990; Hasan and Rigaux, 1991). Moreover, hypoxaemia-
induced elevations in adenosine concentrations transiently inhibit fetal EEG activity during
strong labour contractions and, if the hypoxaemia is severe and protracted enough, EEG activity
may be almost completely suppressed (indicated by an isoelectric trace), an effect which is
usually rapidly reversed if fetal normoxaemia is restored between contractions (Mallard et al.,
1992; Hunter et al., 2003). Likewise, with loss of placental oxygen supply due to severance of the
umbilical cord immediately after birth, the EEG of the newborn would progress towards an
isoelectric state, reached after 60–90 s (Mallard et al., 1992; Hunter et al., 2003), and this would
usually be reversed only when successful breathing begins.
Although an isoelectric EEG trace indicates very marked suppression of activity in the
cerebral cortex, the normal functions of which are required for consciousness to occur, brain stem
function supporting the reflexes involved in the initiation of breathing (among other functions) is
safeguarded, even during protracted periods of hypoxaemia (Jensen et al., 1987). Thus severance
of the umbilical cord and the associated fall in oxygen and rise in carbon dioxide tensions in the
newborn’s blood stimulate gasping, and if the respiratory system is mature enough, this leads to
successful inflation of the lungs, the onset of breathing and a rapid elevation in oxygen tensions
which eventually rise to well above maximum fetal levels (Mellor and Gregory, 2003). This
oxygenation of the newborn, together with the loss of the placental source of adenosine, would
result in a very rapid decrease in circulating and cerebral adenosine concentrations and a decrease
in adenosine suppression of the cerebral cortex. We consider this to be critical for the onset of
consciousness after birth.
52 D.J. Mellor, T.J. Diesch / Applied Animal Behaviour Science 100 (2006) 48–57

Loss at birth of the placental source of allopregnanolone and pregnanolone (and/or of their
precursors) and loss of the placental peptide inhibitor would also contribute to the onset of con-
sciousness in the newborn, but cerebral pregnanolone (and presumably allopregnanolone) con-
centrations do not apparently change much during labour (Nguyen et al., 2003). Accordingly, these
particular neuroactive steriods presumably continue to exert some suppressive effects on the EEG
even after birth. However, a number of EEG activators begin to operate just before and during labour,
especially during the final delivery stage, and immediately after birth (Mellor and Gregory, 2003). In
view of the appearance of consciousness in newborn farm animals shortly after birth (Mellor and
Gregory, 2003; Mellor and Stafford, 2004), the combined stimulatory effects of these activators are
evidently sufficient to overcome any marked residual effects of the suppressors noted above.

5.2. Activators of brain function

The principal activators briefly considered here are 17b-oestradiol, noradrenaline and a
barrage of sensory input associated with birth and entry into the postnatal environment.
17b-oestradiol is a neuroactive steroid, which, in contrast to allopregnanolone and
pregnanolone, has rapid-onset excitatory effects widely within the brain (Wong et al., 1996;
Woolley, 1999; McEwen, 2002). When injected into the fetus or premature newborn it stimulates
arousal behaviour and breathing activity (Mellor and Gregory, 2003). As its fetal plasma
concentrations rise progressively during labour (Challis and Patrick, 1981), 17b-oestradiol
presumably contributes to preparing the brain to support the increase in behavioural activity and
the onset of breathing, which usually occur immediately after birth (Mellor and Gregory, 2003),
and the subsequent appearance of consciousness.
The locus coeruleus extends noradrenaline-releasing nerves widely within the brain from the
cerebral cortex to the brain stem and has major roles in stimulating arousal and alert vigilance, as
reflected in specific EEG states (Svensson, 1987; Berridge and Waterhouse, 2003). The locus
coeruleus-noradrenaline system is particularly responsive to painful stimuli and to hypoxaemia
and hypercapnia (elevated blood carbon dioxide tensions), and is present and operational,
although not particularly active, in the fetus before labour (Joseph and Walker, 1990). However,
strong tactile stimulation (including pain receptor input) associated with head and body
compression during labour, and especially during the final stage before delivery (Mellor and
Gregory, 2003), and the transient episodes of hypoxaemia/hypercapnia associated with labour
contractions and, after birth, with severance of the umbilical cord before breathing starts (see
above), are potent stimuli to the locus coeruleus brain activating effects. These presumably also
prime the brain for the onset of arousal and consciousness very soon after birth.
Immediately after birth the newborn is exposed to air, gravity, hard surfaces, unlimited space
and, usually, to cold challenge for the first time (Mellor and Gregory, 2003), and this will be
associated with a barrage of novel sensory information which is likely to be arousing. Cold
stimulation of skin thermoreceptors in particular is a potent stimulus to both fetal and newborn
arousal and breathing, and tactile stimulation of the head and ears either by maternal licking or
manually by farm staff apparently also has activating effects (Mellor and Gregory, 2003).

6. Integrated summary of suppression and activation of consciousness in the fetus and

newborn

The above analysis suggests that fetuses subjected to normal in utero sensory input remain in
sleep-like (unconscious) states and that awareness appears for the first time only after birth.
 D.J. Mellor, T.J. Diesch / Applied Animal Behaviour Science 100 (2006) 48–57 53

Suppression of fetal consciousness-related EEG activity is evidently achieved by the combined

effects of a high brain adenosine, allopregnanolone/pregnanolone and PGD2 status acting together
with a placental inhibitor (a peptide), warmth, buoyancy and cushioned tactile stimulation. This
suppression continues during labour despite marked rises in the circulating concentrations of 17b-
oestradiol and locus coeruleus-induced noradrenaline release, both of which are putative activators
of behavioural arousal and consciousness. The 17b-oestradiol surge results from the progressive
switch in placental steroidogenesis away from progesterone and begins some days before birth. The
rise in locus coeruleus-induced noradrenaline release, which is apparently particularly marked in the
final stage of labour, is due to stimulation of the locus coeruleus by head and body compression (and
sometimes injury) during passage of the fetus through the cervix and vagina. It is also due to locus
coeruleus responses to acute, usually transient, periods of fetal hypoxaemia/hypercapnia during
uterine contractions. However, as the hypoxaemia would also lead to an increase in brain production
of adenosine and its suppression of EEG activity, the two effects may nullify each other.
After birth, during the period between severance of the umbilical cord and the onset of breathing,
the newborn becomes progressively more hypoxaemic/hypercapnic and the adenosine concentra-
tions of the cerebral cortex would rise markedly, thereby further suppressing its electrical activity,
but at this stage brainstem gasping reflexes evidently remain operational. Studies of reversible
umbilical cord occlusion in near-term fetal sheep show that if the onset of effective breathing after
birth is delayed for about 60–90 s the EEG would become isoelectric (Mallard et al., 1992; Hunter
et al., 2003), an effect which would be rapidly reversed with the onset of breathing. In fact, gasping as
a prelude to regular breathing usually occurs in vigorous newborns within the first minute after birth.
This, and the subsequent onset of regular breathing lead to a rapid rise in circulating, and therefore
tissue, oxygen tensions to well above usual fetal levels (Mellor and Gregory, 2003). This, together
with loss of placental adenosine input, would cause a speedy reduction in brain concentrations of
adenosine and its suppressive effects on EEG activity. This rapid postnatal removal of what is
evidently an overriding suppression by adenosine presumably then allows the activators of the
cerebral cortex to operate. High circulating 17b-oestradiol concentrations and strong stimulation of
the locus coeruleus–noradrenaline system are present during labour and after birth. With the onset of
breathing after birth, they presumably act together with cold stimulation of cutaneous
thermoreceptors and with tactile stimulation through contact with hard surfaces and maternal
licking to promote the first appearance of consciousness. Marked changes in auditory and visual
inputs, which undoubtedly occur at birth (Mellor and Gregory, 2003), may also contribute.
Although adenosine suppression evidently declines very rapidly after birth, some effects of
pregnanolone (and presumably allopregnanolone) are likely to continue at least during the first day,
despite loss of the placenta as a major source of it, because its circulating concentrations are still
significant 3 days after birth (Nguyen et al., 2003). Likewise, the decline in the plasma
concentrations of the placental peptide inhibitor, due to loss of the placenta after birth, would
probably not be as rapid as withdrawal of adenosine suppression. It is likely, therefore, that the
above noted activators are required to overcome residual suppression by allopregnanolone,
pregnanonlone, the placental inhibitor and other agents as their suppressive effects wane after birth.

7. Implications for suffering in the fetus and newborn

7.1. Prior to and during birth

For any animal to suffer it must be both sentient and conscious (see above). The analysis
provided here shows that neurological development is insufficient for sentience until at least half
54 D.J. Mellor, T.J. Diesch / Applied Animal Behaviour Science 100 (2006) 48–57

way through pregnancy, and that the capacity for sentience evident in neurologically mature farm
animals after birth develops during the last half of pregnancy. Nevertheless, even when the
capacity for sentience has developed the fetus remains unconscious, as indicated by its sleep-like
EEG states and the demonstrated operation in utero of a range of neuroinhibitory mechanisms
that actively maintain the fetus asleep. It follows that although one precondition for suffering, i.e.
the capacity for sentience, is met during late pregnancy, the absence of the other precondition, i.e.
consciousness, before birth means that the fetus, and the embryo before it, cannot perceive by the
senses and therefore cannot suffer.
However, there remains the possibility that the fetus might be arousable to a state of
consciousness by noxious stimulation. Three examples will clarify this. First, surgical
interventions in the naturally unconscious (i.e. sleeping) fetus in an anaesthetised dam usually
impede placental gas exchange and thereby cause various degrees of fetal hypoxaemia during and
for some time after the surgery (Mellor and Gregory, 2003), and the associated rise in fetal
cerebral adenosine concentrations would lead to even deeper states of unconsciousness, not
arousal. Second, during slaughter of the dam, the rapid cessation of fetal oxygen supply and the
linked rapid increase in fetal adenosine concentrations acting on the already unconscious fetus
would lead to an isoelectric EEG within 60–90 s (Mallard et al., 1992; Hunter et al., 2003), not
arousal to consciousness. This observation contributed to the development of principles for the
humane slaughter of the fetuses of pregnant ruminants (Mellor, 2003). Third, vibroacoustic
stimulation of the fetus of sufficient intensity to induce movement does not cause the EEG to
change from a sleep-like to an aroused or conscious state (Leader et al., 1988; Abrams et al.,
1996; Bauer et al., 1997; Schwab et al., 2000). These observations suggest that the fetus in utero
is not arousable to a state of consciousness.
Fetal unconsciousness persists throughout labour and may indeed become deeper, partly
through changes that are not related to hypoxaemia (Berger et al., 1986; Shinozuka and
Nathanielsz, 1998) and partly through repeated transient hypoxaemia-adenosine induced
suppression of brain function during intense and/or protracted labour contractions (see above).
Thus, although mechanical and pain receptor nerve pathways will be activated by the marked
compression and, when it occurs, injury, which are associated with labour and delivery, the fetus
is protected from suffering because of its unconscious state. This is reassuring for the conduct of
fetotomy on those occasions when living fetuses need to be dismembered in utero in order to
resolve intractable dystocia (Mellor and Gregory, 2003).

7.2. After birth

The first appearance of consciousness after birth occurs only when breathing oxygenates the
newborn sufficiently to remove the dominant adenosine inhibition of brain function. The
newborn that never breathes will have an isoelectric EEG and will die without suffering. The
newborn that does breathe, but not sufficiently to effect an oxygen-induced reduction in
adenosine to levels compatible with consciousness, will remain unconscious and will die without
suffering. On the other hand, most newborn farm animals become conscious within minutes of
birth through the operation of the mechanisms outlined above. Once conscious, they have the
potential to perceive noxious and other sensations and to suffer if the character, intensity and/or
duration of those sensations are sufficiently noxious or aversive (Mellor and Stafford, 2004).
In their evaluation of the welfare implications of mortality and morbidity in newborn farm
animals Mellor and Stafford (2004) considered that the major noxious subjective experiences of
animal welfare concern are breathlessness, hypothermia, hunger, sickness and pain. Reference to
 D.J. Mellor, T.J. Diesch / Applied Animal Behaviour Science 100 (2006) 48–57 55

documented responses of farm animals and, where appropriate, to human experience, suggested
that breathlessness and hypothermia usually represent less severe neonatal welfare insults than do
hunger, sickness and pain. However, two or more of these experiences can overlap, sometimes
with greater negative welfare consequences (e.g. sickness plus pain), and sometimes where one
mitigates the effects of another (e.g. where hypothermia dulls consciousness in hungry or sick
newborns). Fortunately, major science-based improvements in the management of pregnancy and
birth have markedly reduced the overall amount of welfare compromise experienced by newborn
farm animals (Mellor and Stafford, 2004) and further improvements may be expected as
knowledge is refined and extended in the future.

Acknowledgements

We are particularly grateful to Associate Professors Laura Bennet and Alistair Gunn
(Department of Physiology, University of Auckland), Dr David Walker, Department of
Physiology, Monash University) and Dr David Bayvel (Animal Welfare Group, Ministry of
Agriculture and Forestry, MAF) for helpful discussion on the topics covered here, and to the
Agricultural and Marketing Research and Development Trust and MAF Science Policy for
financial support for related research projects.

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