DC Electrical Stimulation of the Pretectal Thalamusand Its Effects on the Feeding Behaviorof the Toad (Bufo bufo)
James McConville,* Peter R. Laming
School of Biology and Biochemistry, MBC, Queens University of Belfast, Belfast BT9 7BL,United Kingdom
Received 20 September 2006; accepted 5 January 2007
ABSTRACT: The feeding motivation of the com-
mon European common toad (Bufo bufo) can be quanti-
fied by the feeding sequence of arousal-orientation-
approach-fixate-snap. Previous work has found that the
optic tectum is an important structure responsible for
the mediation of feeding behaviors, and combined elec-
trical and visual stimulation of the optic tectum was
found to increase the animals feeding behaviors. How-
ever, the pretectal thalamus has an inhibitory influence
upon the optic tectum and its lesion results in disinhib-
ited feeding behaviors. This suggests that feeding behav-
ior of anurans is also subject to influence from the
pretectal thalamus. Previous studies involving the appli-
cation of DC stimulation to brain tissue has generated
slow potential shifts and these shifts have been impli-
cated in the modulation of the neural mechanisms
associated with behavior. The current study investigated
the application of DC stimulation to the diencephalon
surface dorsal to the lateral posterodorsal pretectal
thalamic nucleus in Bufo bufo, in order to assess effects
on feeding motivation. The application of DC stimula-
tion increased the incidence of avoidance behaviors to a
visual prey stimulus while reducing the prey catching
behavior component of approach, suggesting that the DC
current applied to the pretectum increased the inhibition
upon the feeding elements of the optic tectum. This can
be explained by the generation of slow potential shifts.
' 2007 Wiley Periodicals, Inc. Develop Neurobiol 67: 875–883, 2007
Keywords: Bufo bufo; direct current; feeding;
pretectum; motivation
INTRODUCTION
The feeding behaviors of anurans follow the set se-
quence of ‘arousal-orientation-approach-fixate-snap’
(Eibl-Eibesfeldt, 1951) and the number of times each
component is displayed can be used as a measure-
ment of the animal’s motivation to feed. Of particular
importance to feeding motivation is the presentation
of the ‘worm-like’ visual stimulus (WLS), since the
stomach content of toads (Bufo bufo) have revealed
that these animals feed primarily on beetles, milli-
pedes, slugs, and earthworms (Porter, 1972). This
suggests that objects moving in the same direction as
their longest edge are considered as prey, whereas
movement in the direction of the shortest edge consti-
tutes non-prey and does not elicit a prey catching
response and may even elicit a defensive reaction
(Ewert, 1987). This was verified by presentation of
small elongate artificial prey objects moving in the
same direction as their longest edge, which elicited
feeding behaviors in Hyla arborea, Rana temporaria,Alytes obstetricans, Bufo bufo bufo, Bufo bufo spino-sus, and Bombina variegata, while objects moving
perpendicular to the longest edge did not elicit feed-
ing behaviors and even induced avoidance behaviors
(Ewert, 1969)
Visual input in anurans is integrated by the optic
tectum and has been extensively investigated by AC
Correspondence to: J. McConville ([email protected])
' 2007 Wiley Periodicals, Inc.Published online 21 February 2007 in Wiley InterScience (www.interscience.wiley.com).DOI 10.1002/dneu.20390
875
stimulation (Roitbak et al., 1992) and presentation of
visual stimulation (Laming and Ewert, 1984a; Ewert,
1989; Laming et al., 1995; McConville et al., 2006).
Within the optic tectum, the nature of visual objects
is determined primarily through the activity of the
tectal T5 cells consisting of the T5 (1), T5 (2), and T5
(3) subtypes. T5 (1) subunits respond maximally to
objects moving in the same direction as its longest
edge and T5 (3) subunits respond maximally to exten-
sion perpendicular to movement. However, T5 (2)
subunits integrate and interpret visual input in that
they are sensitive to both types of objects (Laming,
1992). These prey selective cells also have input to
the medulla via tecto-bulbar tracts, suggesting that
they have a major influence upon response generation
(Satou and Ewert, 1984).
There is also a close cellular relationship between
the optic tectum and the pretectal thalamus (Szekely
and Lazar, 1976; Wilczynski and Northcutt, 1983a,b;
Schwippert et al., 1995) in that the pretectal thalamus
exerts a degree of inhibition upon the optic tectum
(Ewert, 1974, 1983, 1989; Ewert et al., 1979, 1983;
Buxbaum-Conradi and Ewert, 1995) as shown by
disinhibited feeding induced by pretectal thalamic
lesions (Laming and Ewert, 1982). Disinhibition of
feeding behavior by pretectal lesions largely involves
the prey selective tectal T5 (2) cells, since prectecal
lesion also results in increased firing rate and de-
creased selectivity of the T5 (2) cells (Ewert, 1967,
1968; Ewert et al., 1974; Laming and Ewert, 1982).
The pretectal inhibition is generated by the activity of
TH3 cells within the pretectal thalamus, which are
analogous to the non-prey sensitive tectal T5 (3) cells
in that they are maximally responsive to non-prey
objects (Ewert et al., 1983).
The present investigation aims to determine if DC
stimulation of the diencephalon surface just dorsal to
the lateral posterodorsal thalamic nucleus (Lpd) has
an effect on toads’ (Bufo bufo) feeding behavior.
Applied AC and DC electrical current to the anuran
optic tectum results in ionic fluxes recorded as slow
potential shifts (SPS) (Roitbak et al., 1987, 1992;
Laming, 1992; Laming et al., 1992; Sterritt et al.,
2000) and there is a wealth of knowledge suggesting
that SPS’s have a significant impact on neural
function. This is because SPS reflect movement of
potassium ions through glial cells which modulate
neuronal function with obvious implications for
behavior (Ransom, 1973a,b,c; Laming, 1983, 1989,
2000; Laming et al., 1984a,b, 1995; Roitbak et al.,
1987, 1992).
Compared to that on AC stimulation, relatively
little work has been conducted on the behavioral
effects of DC stimulation applied to brain structures
especially on the anuran pretectal thalamus, but
previous investigations have found that DC stimula-
tion applied to the surface of brain tissue induces
SPS’s (Sterritt et al., 2004). This induction of ionic
fluxes through glial cells may be done without neces-
sarily stimulating neurons, giving a purer reflection
of the effects of SPS’s.
This current study found that as the current applied
increased feeding behaviors decreased and avoidance
behaviors increased when presented with a prey like
object. The stimulation may be having an effect on
the TH3 cells/cell populations in the pretectal thala-
mus associated with visual stimulus recognition via
generation of SPS’s, increasing inhibition upon the
prey selective functions of the optic tectum.
METHODS
Animals
Adult toads (Bufo bufo) obtained from a commercial
supplier were maintained in vivaria for at least a month
prior to the experiment, being fed twice a week on meal-
worm (Tenebrio molitor) larvae. Ten male toads were
selected for experimentation and all experiments and
animal conditions were subject to the Animals (Scientific
Procedures) Act 1986.
Behavioral Testing
Toads were placed on a 20 3 20 cm2 crystallizing dish
painted white apart from 10-cm transparent window. The
dish was placed in the center of a box with a turntable under
a fixed base to allow a piece of black cardboard 3 cm long
3 0.75 cm to be rotated around the dish at �2 cm/s as a
‘worm like’ stimulus (WLS). The WLS could then be pre-
sented both clockwise and anti-clockwise around the dish,
i.e., left to right and right to left, respectively, from the
toad’s perspective. The box measured 40 3 40 3 40 cm3,
and the inside was painted white to give a homogeneous
background and optimal contrast (McConville et al., 2006),
see Figure 1.
Electrode Preparation
Teflon-coated platinum Iridium wire of 0.0125 mm diame-
ter was cut into 2.5 cm lengths. One end of the wire was
heated in a flame until a �1-mm ball formed. The other end
was gently scraped with a razor blade to remove a �1 cm
length of the Teflon insulation all around the wire. A length
of 0.6-mm diameter resin insulated copper lead also had a
similar length of the resin insulation scrapped off and the
two wires were then twisted together at these insulation free
points and soldered together to form a stimulation lead
(Fig. 2).
876 McConville and Laming
Developmental Neurobiology. DOI 10.1002/dneu
Two of these leads were then twisted together to form a
lightweight cable of two electrodes and fashioned into a he-
lix. Above the experimental box a supporting horizontal
length of wire was suspended with a swivel attached. To
this the copper cable and ball electrode assembly was fixed
vertically, and the electrodes were surgically fixed to the
cranium; see Figure 1.
Operations
Toads were anesthetized by ether inhalation until breathing
ceased and were covered with a moist tissue to aid cutane-
ous respiration. The temperature of the room was thermo-
statically controlled at (15 6 1)8C. The skin overlying the
cranium was removed using fine curved scissors and the
cranium over the diencephalon was thinned by buffing
the surface with a dental burr to make a transparent
window. This allowed the position of the surface overlying
the lateral posterodorsal thalamic nucleus (Lpd) to be
checked before drilling. A �2 mm diameter burr hole was
drilled over the Lpd/Thalamus surface and ball electrodes
were placed in the hole making contact with the thalamus
surface and secured to the skull with a drop of Permabond
adhesive. The electrode delivering positive polarity DC
stimulation always contacted the right side of the thalamus
overlying the Lpd (Fig. 3). A layer of tissue paper soaked
with water covered the base of the crystallizing dish and the
toad was placed in the dish and allowed to recover for 24 h.
Electrode positioning was verified by examining the brain
post mortem, whereby the cranium was carefully removed
and the proximity of the burr hole to the thalamus surface
determined.
Experiments
Ten animals were used to assess the effects of DC currents.
A Grass photoelectric stimulus isolation unit (PSIU6) fitted
to a Grass S44 stimulator provided the DC stimulation. The
order of all possible current strength and WLS direction
configurations (two per individual current strength) were
presented randomly to reduce order effects with the excep-
tion of zero current, which was always first and the highest
current, which was always given last. This meant that each
toad was subject to 14 stimulation events. DC current was
applied for 10 s while the WLS passed the window of the
dish and the remote presentation of the visual stimulus was
�2 s after initiation of the DC current. The stimulation
events were separated by a 5-min interstimulus period. The
DC stimuli were 0, 0.1, 1, 10, 50, 100, and 300 lA. The
current range applied was chosen to cover a large range of
stimulation while remaining low in order to reduce the pos-
sibility of tissue damage. Sterrit et al. (2004) applied 1 mV
of DC stimulation to induce slow potential shifts in the toad
optic tectum. The magnitude of the SPS’s were greatly
reduced in the posterior tectum compared to anterior
records, which were nearer the stimulation electrode. Ranck
(1975) found that 55–80 lA AC stimulation elicited neuron
responses at a maximum distance of 1090 lm. Quick and
Laming (1988) used similar techniques to asses the current
spread of applied pulsed currents ranging from 0.1 to
200 lA to the surface of the goldfish telencephalon and
optic tectum and found that the maximum distance at which
current spread would excite tectal neurons was a longditudi-
nal distance of 95.5 6 11.16 lm.
The animal’s behavior was observed by the experimenter
from above the testing arena. This was deemed appropriate
since this was the normal method by which the animals
were fed in the vivarium prior to testing.
The results were analyzed by the multivariate analysis
of variance technique (MANOVA) using the statistical
package for the social sciences (SPSSx) (SPSSx Inc., 1986).
Figure 1 Experimental chamber (Laming, 1992). [Color
figure can be viewed in the online issue, which is available
at www.interscience.wiley.com.]
Figure 2 Electrode preparation. [Color figure can be viewed in the online issue, which is available
at www.interscience.wiley. com.]
Pretectal Thalamus and Feeding Behavior 877
Developmental Neurobiology. DOI 10.1002/dneu
The Pillais trace calculation was used for averaged multivar-
iate tests of significance. These calculations are denoted in
the form PF (df1, df2) ¼ F, p ¼ sig, where df1 and df2 are
the numerator and denominator, respectively. From this the
variables responsible for the significance of the multivariate
test (Pillais) was determined by univariate F-tests, denoted
by F (df1, df2) ¼ F, p ¼ sig. SPSSx. Averaged univariate F-
tests are defined by Avf (df1, df2) ¼ X, p ¼ sig, where df1and df2 are the numerator and denominator, respectively.
The number of times each behavior was observed
per 10-s stimulation event constituted the ‘Response Fre-
quency.’ The following behaviors were observed and found
to be statistically significant.
1. Arousal: Nondirectional elevation of the head and
extension of the forelimbs.
2. Approach: Actual movement of the animal towards
the WLS.
3. Retreat: Backwards moving away from the WLS.
4. Crouch: Lowering of head and shoulders.
5. Misdirected orientation/approach: Orientation and/
or approach in the opposite direction of the WLS
propagation.
RESULTS AND ANALYSIS
The effect of current within subjects averaged multi-
variate tests of significance were significant [PF
(36, 324) ¼ 2.6, p < 0.001] and this was attributed to
arousal [F (6, 54) ¼ 2.9 p < 0.05] (Fig. 4), approach[F (6, 54) ¼ 2.7, p < 0.05] (Fig. 5), retreat [F (6, 54)
¼ 23.1, p < 0.001] (Fig. 6), and crouch [F (6, 54) ¼18, p < 0.001] (Fig. 7).
When behaviors were analyzed individually, aver-
aged test of significance involving current within
subjects effects also found that arousal [Avf (6, 54)
¼ 2.9, p < 0.05] (Fig. 4), approach [Avf (6, 54) ¼2.7, p < 0.05] (Fig. 5), retreat [Avf (6, 54) ¼ 23.1,
p < 0.001] (Fig. 6) and crouch [Avf (6, 54) ¼ 18,
p < 0.001] (Fig. 7) were all significant.
Increased DC stimulation elicited a mostly constant
arousal response albeit with a decrease at 0.1 and
50 lA (Fig. 4). Increased DC stimulation decreased
the approach response up until a stimulation of
300 lA, where there is a small increase in response
frequency (Fig. 5). The retreat and crouch responses
were not evident at currents less than 100 lA but
increased between 100 and 300 lA (see Figs. 6 and 7,
respectively). The figures show bar graphs of the
mean response frequency of each behavior and asso-
ciated þ standard error mean (SEM) bars per 10-s
stimulation event.
DISCUSSION
DC stimulation of the dorsal surface of the lateral
posterodorsal thalamic nucleus (Lpd) in Bufo bufo
Figure 4 Every stimulation event generated the arousal
response albeit with much lower values at 0.1 and 50 lA.
[Color figure can be viewed in the online issue, which is
available at www.interscience.wiley.com.]
Figure 3 The position of the frontal telencephalon, cen-
tral diencephalon over Lpd, and rear optic tectum (Laming,
1992). [Color figure can be viewed in the online issue,
which is available at www.interscience.wiley.com.]
878 McConville and Laming
Developmental Neurobiology. DOI 10.1002/dneu
results in a relatively constant arousal response and a
decrease in the frequency of the ‘approach’ feeding
behavior, albeit with an increase at 300 lA and this
may be evidence of a novel behavior to predators.
The increase in the approach response at 300 lA may
be evidence of some initial precursory movements
associated with responses to predators in which toads
will sometimes freeze and turn towards snakes and
expose their flanks in a stiff legged stance (Ewert and
Traud, 1979).
On the other hand, increased DC stimulation
increased the frequency of the avoidance behaviors,
‘retreat’ and ‘crouch’. This suggests a shift in how
the animal is interpreting the visual stimulus in that at
higher DC current the prey like visual stimulus is
being interpreted as predatory at the expense of feed-
ing behavior.
The optic tectum is the primary integrative center
of visual input in anurans, where a number of tectal
cells interpret and process visual information. ‘T5’
cell types within the optic tectum and its three sub-
types are primarily responsible for the interpretation
of moving visual objects to determine if they are prey
or non-prey (Ewert et al., 1979, 1983; Ewert, 1983,
1987). T5 (3) cells respond maximally to visual stim-
uli moving perpendicular to its longest edge, i.e., an
antiworm stimulus and T5 (1) cells respond maxi-
mally to visual stimuli moving parallel to its longest
edge and movement perpendicular to the longest
edge, i.e., both worm like and non-worm configura-
tions (Ewert et al., 1979, 1983; Ewert, 1983, 1987).
The T5 (2) cells represent a functional unit of visual
stimulus perception as they respond maximally to
prey like configurations and since T5 (2) cells can be
antidromically stimulated from the medulla the T5
(2) cells translate the processed sensory information
to motor activity via the tecto/bulbar tracts (Satou
and Ewert, 1984).
The pretectal thalamus has a significant input to
the optic tectum (Wilczynski and Northcutt, 1983a,b),
which has an inhibitory influence upon the prey selec-
tive elements of the optic tectum as seen by disinhib-
ited feeding responses resulting from pretecal lesions
(Ewert, 1967, 1968; Ewert et al., 1974; Laming and
Ewert, 1982). Within the pretectal thalamus ‘TH3’
cells respond primarily to large moving stimuli and
are found predominantly in the Lpd and lateral poste-
rior (P) pretectal regions. Since the pretectal neuropil
receives retinal input from a number of retinal
Figure 6 An increase in current intensity results in an
increase in the retreat response frequency. The behavior is
not displayed at all at currents less than 100 lA. [Color fig-
ure can be viewed in the online issue, which is available at
www.interscience.wiley.com.]
Figure 5 Increased DC stimulation decreases the ap-
proach response. [Color figure can be viewed in the online
issue, which is available at www.interscience.wiley.com.]
Pretectal Thalamus and Feeding Behavior 879
Developmental Neurobiology. DOI 10.1002/dneu
ganglion cells, such visual input would activate the
TH3 cells, increasing their activity and as a result the
inhibitory output to the tectum (Ewert, 1987, 1989;
Schwippert et al., 1995).
AC electrical stimulation of the pretectal thalamus
temporarily inhibits the activity of the prey selective
tectal T5 (2) cells, which proves that electrically
induced increases in activity of the pretectal thalamus
inhibits the prey selective function of the optic tectum
(Ewert et al., 1974).
There is also an inhibitory influence from the
telencephalon upon the pretectal thalamus as shown
by ablation of the telencephalon, resulting in feeding
behaviors failing to occur, whereas subsequent pre-
tectal ablation results in disinhibited feeding behav-
iors (Ewert, 1968, 1987). A striato-pretecto-tectal
feedback loop via the lateral forebrain bundle (LFB)
and lateral anterior thalamus provides a neural basis
for a more global modulation of the feeding behavior
of amphibians (Wilczynski and Northcutt, 1983a,b).
Matsumoto et al. (1991) examined intracellular re-
cordings from the Lpd/P region of the pretectal thala-
mus in response to electrical stimulation of the caudal
ventral striatum (vSTR) or ipsilateral LFB. The study
found pure IPSP’s from the striatum to the Lpd/P as
previously suggested by ablation studies. A more
recent work by Buxbaum-Conradi and Ewert (1995)
investigated the activity of the caudal ventral striatum
(vSTR) in visuomotor activity of Bufo marinus. A
number of striatal cell types were defined in terms of
responses to visual and electrical stimulation of the
LFB. The study found that 40% of the responses to
LFB stimulation were striatal efferents and this could
innervate the optic tectum by striato-pretecto, striato-
tegmento, and/or striato-pallio-pretecto-tectal path-
ways. This suggests that the vSTR may also be modu-
lating the perceptual and motor aspects of amphibian
visual attention.
The present study was conducted to determine the
effects of pretectal DC stimulation upon the anuran
feeding behaviors, since relatively little work had
been undertaken with direct current, with most work-
ers employing AC stimulation. To our knowledge, no
work had been undertaken using simultaneous DC
stimulation of the anuran pretectal thalamus and pre-
sentation of prey like objects. The results of the pres-
ent study suggest that increased DC stimulation
increased the activity of the Lpd region of the pretectal
thalamus, increasing the inhibitory input to the prey
selective processes in the optic tectum. This increased
inhibition on the optic tectum resulted in increased
avoidance behavior at the expense of feeding or prey
catching behaviors to the visual stimulus and the WLS
being interpreted as non-prey or predator. The precise
mechanisms of how DC stimulation produced this
shift in motivation are not clear from the current study
but previous studies using DC electrical stimulation of
anuran brain tissue generated slow potential shifts
(SPS) (Sterritt et al., 2004). SPS’s are a manifestation
of the depolarizing movement of potassium ions
through glial cells (King, 1960; Ransom and Goldring,
1973b,c; Gardner-Medwin, 1983, 1987; Laming,
1983, 1989, 2000; Laming and Ewert, 1984a,b; Roit-
bak et al., 1992) and there is evidence that SPS polarity
and amplitude are associated with changes in motiva-
tional state in many species (Laming, 1983, 1992,
2000; Laming and Ewert, 1984a,b; Quick and Laming,
1990; Laming et al., 1995).
Neuron resting potentials are dependent on lower
extracellular potassium concentrations, and propagat-
ing action potentials are a depolarization of the
neuron membrane with expulsion of potassium into
the extracellular milieu. Increased extracellular potas-
sium reduces neuronal firing thresholds by depolariz-
ing the membrane close to that required for the gener-
ation of action potentials priming cells and increasing
the likelihood of action potential generation (Laming,
1983, 2000; Laming and Ewert, 1984a). Application
of potassium to the brain resulted in an increase in
the unit and SPS responses from the optic tectum of
Figure 7 An increase in current intensity results in an
increase in the crouch response frequency. The behavior is
not displayed at all at currents less than 100 lA. [Color fig-
ure can be viewed in the online issue, which is available at
www.interscience.wiley.com.]
880 McConville and Laming
Developmental Neurobiology. DOI 10.1002/dneu
non-hungry toads to a square visual stimulus (Laming
and Laming, 2004).
In mammals the SPS closely matches the reloca-
tion of potassium by astrocytic glia, suggesting that
astrocytic movement of potassium ions is responsible
for the recorded SPS. Glial cells readily take up
potassium, and since neurons expel potassium during
action potential generation, these ions will be taken
up by the surrounding glia. The potassium ions will
then flow through the glial cells along concentration
gradients to be expelled into regions of extracellular
space of comparatively lower ion concentration, i.e.,
areas of relatively lower neuronal activity (Gutnick,
et al., 1981; Gardner-Medwin, 1983, 1987; Roitbak
et al., 1987, 1992). Gap junctions between astrocytes
offer a pathway of reduced resistance to ion flow,
making it possible for the potassium to flow through
glia and down concentration gradients faster than
action potentials can propagate across synapses
(Gutnick et al., 1981; Gardner-Medwin, 1983, 1987).
In addition, glial cells and neurons engage in an inti-
mate physiological relationship during cell maturation
(King, 1960; Rakic, 1974; Hatten, 1990; Cameron
and Rakic, 1994). The preservation of these ontogenic
relationships results in a ‘functional syncytium,’
where relocation of potassium may ‘prime’ function-
ally related populations of neurons, offering a poten-
tial mechanism of modulation of motivation through
the relocation of potassium to cells in imminent
receipt of input before the input arrives.
Anuran brain tissues have considerably less astro-
cytes but are heavily invested with radial glia, which
are long single processes and these glial cells offer
a similar low resistance pathway to ions and may
account for the SPS recorded at depth and across
anuran brain tissues (Laming, 1983, 1992, 2000; Lam-
ing and Ewert, 1984a,b; Roitbak et al., 1992; Laming
et al., 1995; Laming and Laming, 2004; Sterritt et al.,
2004).
Experiments by Laming and Ewert (1984a) carried
out on conscious but immobilized toads elicited
monophasic SPS responses as well as visual unit and
EEG responses to simulated natural prey objects. At
the tectal surface, the unit activity preceded EEG and
SPS changes, but in the deeper layers of the sensory
processing system, the SPS preceded the EEG change
and significantly pre-empted the activity of the local
units, suggesting a faster transfer of potassium ions
through radial glia, than action potential propagation
(Laming and Ewert, 1984a).
Investigations involving the application of DC
stimulation to anuran brain surface tissues have also
elicited SPS’s. Sterritt et al. (2004) applied DC stimu-
lation to the surface of the optic tectum of toads
(Bufo bufo) as well as presenting visual prey like
object similar to those presented here. The anterior
tectum is the primary input area for the optic tectum
and negative SPS responses from the anterior tectum
reflected the animal’s prior motivation to feed. This
negative SPS was associated with a positive SPS in
the posterior tectum and the movement of the animals
resulted in a reversal of polarity, suggesting that
movement itself activates large swathes of the tectum
and activates many sinks and sources of potassium
both tangentially and radially through the optic
tectum (Laming et al., 1995; Sterritt et al., 2004). DC
stimulation of the optic tectum also resulted in SPS
responses of similar polarity and rebound responses
as with visual stimulation albeit of a greater magni-
tude. The SPS were generated by the DC stimulation
and summated with the SPS associated with the prior
feeding motivation to enhance the neuronal
responses, especially with the negative phase of the
SPS (Sterritt et al., 2004). Experiments have also
been conducted by applying DC stimulation to the
optic tectum of toads, which increased feeding
responses and avoidance responses, suggesting a
more global activation of neuronal cells and potas-
sium sinks (McConville, 2006). Experiments apply-
ing DC stimulation to the scalp in humans affects
cortical activity and even improves learning func-
tions, and this may well be due to the modulatory
effects of SPS’s (Nitsche and Paulus, 2000; Nitsche
et al., 2002; Marshall et al., 2004).
In the current situation, DC stimulation-induced
SPS’s may be relocating potassium ions, via radial
glia, to layers of the pretectal thalamus housing the
non-prey selective TH3 cells before the onset of the
local neuronal response. Priming of these cells prior
to input would increase their likelihood of action
potential generation and at a population level increase
the inhibitory output to the prey selective elements
of the optic tectum. This may well account for the
increase in avoidance behaviors to prey like objects
evidenced in the current study.
REFERENCES
Buxbaum-Conradi H, Ewert JP. 1995. Pretecto-tectal
influences—What the toads pretectum tells its tectum:
Antidromic stimulation/recording study. J Comp Physiol
176:169–180.
Cameron RS, Rakic P. 1994. Identification of membrane
proteins that comprise the plasmalemal junction between
migrating neurons and radial glial cells. J Neurosci 14:
3038–3055.
Eibl-Eibesfeldt I. 1951. Nahrungserwerb und Beuteschema
der Erdkrote (Bufo bufo). Behaviour 4:1–34.
Pretectal Thalamus and Feeding Behavior 881
Developmental Neurobiology. DOI 10.1002/dneu
Ewert JP. 1967. Untersuchungen uber die Anteile zentral-
nervoser Aktionen an der taxisspezifischen Ermundung
beim Beutefang der Erdkrote (Bufo bufo). Zeitschrift Fur
Vergleichende Physiologie 57:263–288.
Ewert JP. 1968. Der Einflub von Zwisschenhirndefekten
auf die Visuomotorik im Beute-und Fluchtverhalten
der Erdkrote (Bufo bufo). Zeitschrift Fur Vergleichende
Physiologie 61:41–70.
Ewert JP. 1969. Quantatative analyses von reiz-reaktions-
beziehungen bei visullem auslosen der Beutefang-
Wenderreaktion der Erdkote (Bufo bufo L). Pflugers Arch
ges Physiol 308:225–243.
Ewert JP. 1974. The neural basis of visually guided be-
haviour. In: Held R, editor. Recent Progress in Percep-
tion. Readings in Scientific American. San Francisco, CA:
Freeman, pp 96–104.
Ewert JP. 1983. Tectal functions underlying prey-catching and
predator avoidance behaviors in toads. In: Vanegas H,
editor. Neurology of the Optic Tectum. New York: Plenum,
pp 247–416.
Ewert JP. 1987. Neuroethology of releasing mechanisms:
Prey catching in toads. Behav Brain Sci 10:337–405.
Ewert JP. 1989. The release of visual behaviour in toads:
Stages of parallel/hierarchical information processing.
In: Ewert JP, Arbib MA, editors. Visuomotor Coordi-
nation, Amphibians, Comparisons, Models, and Robots.
New York: Plenum, pp 39–109.
Ewert JP, Borchers HW, Weitersheim AV. 1979. Direc-
tional sensitivity, invariance and variability of tectal T5
neurons in response to moving configurational stimuli in
the toad (Bufo bufo). J Comp Physiol 131:191–201.
Ewert JP, Burghagen H, Schurg-Pfeiffer E. 1983. Neuroe-
thological analysis of the innate releasing mechanism
for prey-catching behaviour in toads. In: Ewert JP,
Capranica R, Ingle D, editors. Advances in Vertebrate
Neuroethology. London: Plenum, pp 413–475.
Ewert JP, Hock FJ, Weitersheim AV. 1974. Thalamus/
Praetectum/Tectum: Retinale Topographie und phy-
siolische Interaktionen bei der Krote (Bufo bufo). J Comp
Physiol 92:333–346.
Ewert JP, Traud R. 1979. Releasing stimuli for antipredator
behaviour in the common toad (Bufo bufo L). Behaviour
68:170.
Gardner-Medwin AR. 1983. Analysis of potassium dy-
namics in mammalian brain tissue. J Physiol 325:383–
426.
Gardner-Medwin AR. 1987. Assessment of the glial spatial
buffer mechanism in rat brain, frog brain and retina. In:
Roitbak AI, editor. Functions of Neuronglia. Tiblisi, USSR:
Metsniereba press, pp 137–145.
Gutnick MJ, Connors BW, Ransom BR. 1981. Dye coupling
between glial cells in the guinea pig neocortical slice.
Brain Res 213:486–492.
Hatten ME. 1990. Riding the glial monorail: A common
mechanism for glial-guided neuronal migration in differ-
ent regions of the developing mammalian brain. Trends
Neurosci 13:179–184.
King JG. 1960. Comparative investigation of neuroglia in
representative vertebrates. J Morph 119:434–466.
Laming GE, Laming PR. 2004. Tectal responses to potas-
sium loads and subsequent visual stimuli are affected by
motivational state in the toad. Bufo bufo. Comp Biochem
Physiol A 137:665–674.
Laming PR. 1983. Relationship between the responses of vis-
ual units, EEGs and slow potential shifts in the tectum of
the toad Bufo bufo. In: Ewert JP, Capranica RR, Ingle DJ,
editors. Advances in Vertebrate Neuroethology. London:
Plenum, pp 595–603.
Laming PR. 1989. Do glia contribute to behaviour? A
neuromodulatory review. J Comp Physiol 94:555–568.
Laming PR. 1992. Information processing and neuromodu-
lation in the visual system of frogs and toads. Network
3:71–88.
Laming PR. 2000. Potassium signalling in the brain: Its role
in behaviour. Neurochem Int 36:271–290.
Laming PR, Ewert JP. 1982. The effects of pretectal lesions
on neuronal, sustained potential shifts and EEG respon-
ses of the toads tectum to presentation of a visual stimu-
lus. Comp Biochem Physiol A 76:247–252.
Laming PR, Ewert JP. 1984a. Visual unit, EEG and
sustained potential shift responses to biologically signifi-
cant stimuli in the brains of toads (Bufo bufo). J Comp
Physiol 154:89–101.
Laming PR, Ewert JP. 1984b. Visual unit, EEG and sus-
tained potential shift responses in the brains of toads
(Bufo bufo) during alert and defensive behaviour. Physiol
Behav 31:463–468.
Laming PR, Ocherashvili IV, Nicol AU. 1992. Dendritic
and sustained shifts in potential to electrical stimulation
of the anuran tectal surface. Comp Biochem Physiol A
101:91–96.
Laming PR, Ocherashvili IV, Nicol AU, Roughan JV,
Laming BA. 1995. Sustained potential shifts in the toad
tectum reflect prey catching and avoidance behaviour.
Behav Neurosci 109:150–160.
Marshall L, Molle M, Hallschmid M, Born J. 2004. Trans-
cranial direct current stimulation during sleep improves
declarative memory. J Neurosci 24:9985–9992.
Matsumoto N, Schwippert WW, Beneke TW, Ewert JP.
1991. Forebrain-mediated control of visually guided
prey-catching in toads: Investigation of striato-pretectal
conncetions with intracllular recording/labelling meth-
ods. Behav Processes 25:27–40.
McConville JR, Sterritt L, Laming PR. 2006. Behavioural
responses to electrical and visual stimulation of the toad
tectum. Behav Brain Res 170:15–22.
Nitsche MA, Liebetanz D, Tergau F, Paulus W. 2002. Mod-
ulation of cortical excitability in man using transc-
ranial direct current stimulation. Nervenarzt 73: 332–
335.
Nitsche MA, Paulus W. 2000. Excitability changes induced
in the motor cortex by weak transcranial direct current
stimulation. J Physiol 527:633–639.
Porter KR. 1972. Herpetology. Philadelphia: WB Saunders.
Quick IA, Laming PR. 1988. Cardiac, ventillatory and
behavioural arousal responses evoked by electrical brain
stimulation in the goldfish (Carassius aurarus). Physiol
Behav 43:715–727.
882 McConville and Laming
Developmental Neurobiology. DOI 10.1002/dneu
Quick IA, Laming PR. 1990. Relationship between ECG,
EEG and SPS responses during arousal in the goldfish
(Carassius auratus). J Comp Physiol A 95:459–471.
Ranck JB. 1975. Which elements are excited in electrical
stimulation of mammalian central nervous system: A
review. Brain Res 98:417–440.
Ransom BR, Goldring S. 1973a. Ionic determinants of
membrane potential of cells presumed to be radial glia in
cerebral cortex of cat. J Neurophysiol 36:855–868.
Ransom BR, Goldring S. 1973b. Slow depolarisation in
cells presumed to be radial glia in cerebral cortex of cat.
J Neurophysiol 36:869–878.
Ransom BR, Goldring S. 1973c. Slow hyperpolarisation in
cells presumed to be radial glia in the cerebral cortex of
the cat. J Neurophysiol 36:879–892.
Rakic P. 1974. Emergence of neuronal and glial cell lineages
in primate brain. In: Black IB, editor. Cellular and Molec-
ular Biology of Neuronal Development. New York:
Plenum, pp 28–50.
Roitbak AI, Fanardjhyan VV, Melkonyan DS, Melkonyan
AA. 1987. Contribution of radial glia and neurons to the
surface negative potentials of the cerebral cortex during
its electrical stimulation. Neurosci 20:1057–1067.
Roitbak AI, Ocherashvili IV, Laming PR, Roitbak TA.
1992. Stimulus evoked sustained potential shifts and
changes in extracellular potassium concentration of the
frog optic tectum. J Comp Physiol 170:317–323.
Satou M, Ewert JP. 1984. Specification of tecto-motor
outflow in toads by antidromic stimulation of tecto-
bulbar-spinal pathways. Naturwissenschaften 71:52.
Schwippert WW, Beneke TW, Ewert JP. 1995. Pretecto-
tectal influences B—How retinal and pretectal inputs to
the toads superficial tectum interact: A study of electri-
cally evoked field potentials. J Comp Physiol 176:181–
192.
Sterritt L, Laming G, Laming PR. 2004. Neuronal responses
are differentially affected by the polarity of tectal DC
stimulation in the toad (Bufo bufo). Comp Biochem
Physiol 138:467–474.
Szekely G, Lazar GY. 1976. Cellular and synaptic architec-
ture of the optic tectum. In: Llinas R, Precht W, editors.
Frog Neurobiology. Berlin: Springer, pp 297–385.
SPSSx Inc. 1986. Statistical Package for the Social Scien-
ces. New York: McGraw Hill.
Wilczynski W, Northcutt RG. 1983a. Connections in the
bullfrog striatum: Efferent projections. J Comp Neurol
214:333–343.
Wilczynski W, Northcutt RG. 1983b. Connections of the
bullfrog striatum: Afferent connections. J Comp Neurol
214:321–332.
Pretectal Thalamus and Feeding Behavior 883
Developmental Neurobiology. DOI 10.1002/dneu