Somatodendritic processing - Neuron signalling

1. C H A P T E R
285
Cellular and Molecular Neurophysiology. DOI: 10.1016/B978-0-12-397032-9.00013-3
Copyright © 2015 Elsevier Ltd. All rights reserved
13
Somato-dendritic processing
of postsynaptic potentials I: Passive
properties of dendrites
Constance Hammond
Neurons of the mammalian central nervous system
receive many afferents which contact different parts of
their somato-dendritic arborization. When these affer-
ents are activated, if their combined effect is depolarizing
enough, they trigger the firing of sodium action potentials
in the postsynaptic neuron. Classically, it is accepted that
these action potentials are generated at a central point in
the neuron, at the level of the initial segment of the axon
(action potential generating zone; see Section 4.4.3 and
Figure 13.1). The action potential propagates back to the
soma and forward to the axon and axon terminals.
Action potentials are the response of the postsynaptic
neuron. This response may be simple, consisting of a sin-
gle action potential. In this case, it can be described by a
single characteristic: its latency. However, the postsynaptic
response is generally more complex, consisting of several
action potentials. It can then be described by several pa-
rameters: the latency of the first action potential, the dura-
tion of the response, the frequency of the action potentials
that compose the response and the overall form – the pat-
tern or configuration – of the response (see Figure 14.1).
The events that lead to a postsynaptic response can be
separated into several stages. When the afferent synapses
are activated, an excitatory or inhibitory current is gener-
atedatthesubsynapticmembrane,asaresultofactivation
of receptor channels by the neurotransmitter(s). These
postsynaptic currents propagate through the dendrites
to the soma and to the initial segment of the postsynaptic
neuron. In the course of their propagation, the postsyn-
aptic currents summate. If the sum of the postsynaptic
currents is sufficient to depolarize the membrane of the
initial segment as far as the threshold potential for activa-
tion of the voltage-sensitive sodium channels, a response
is triggered in the postsynaptic neuron (Figure 13.1).
However, we will see in the following chapters that
the presence of a postsynaptic response and the char-
acteristics of this response are not the result only of the
integration of different currents of synaptic origin over
the somato-dendritic tree. In fact, the response of the
postsynaptic neuron is the result of two types of cur-
rents: currents across receptor channels in the postsyn-
aptic membrane evoked by neurotransmitters and cur-
rents across voltage-sensitive channels present in the
non-synaptic membrane. Currents of the first type are
generated strictly at the postsynaptic membrane and
their presence and duration is determined essentially by
the interaction between the transmitter and the recep-
tor channel and the intrinsic properties of the receptor
channel. Currents of the second type are generated at the
non-synaptic membrane (dendritic, somatic or at the ini-
tial segment) by voltage changes resulting from currents
of synaptic origin, or from currents generated during
the first action potential that is fired. The voltage-gated
channels responsible for this second type of current are
O U T L I N E
13.1 Propagation of excitatory and inhibitory
postsynaptic potentials through
the dendritic arborization 286
13.2 Summation of excitatory and inhibitory
postsynaptic potentials 288
13.3 Summary 292
Further reading 292

2. 286 13. Somato-dendritic processing of postsynaptic potentials I: Passive properties of dendrites
III. Somato-Dendritic Processing and Plasticity of Postsynaptic Potentials
different from those of the sodium action potential and
are generally activated in the sub-threshold range of
membrane potentials. The duration of these subliminal
voltage-gated currents is determined by the gating prop-
erties of the corresponding channels.
This chapter looks at the conduction and the sum-
mation of synaptic currents (first type of currents) over
the dendritic tree. The characteristics of the diverse non-
synaptic, subliminal currents (second type of currents)
together with their role in the pattern of the postsynaptic
discharge will be studied in the following chapters.
13.1 PROPAGATION OF EXCITATORY
AND INHIBITORY POSTSYNAPTIC
POTENTIALS THROUGH THE
DENDRITIC ARBORIZATION
Excitatoryandinhibitorypostsynapticpotentialsresult,
respectively, from depolarizing or hyperpolarizing cur-
rents through channels opened by neurotransmitters (re-
ceptorchannels)inthepostsynapticmembrane.Thesecur-
rents are generated over the somato-dendritic tree, at sites
more or less distant from the soma (distal dendritic sites or
proximal dendritic sites). Once generated, the postsynap-
tic currents propagate along the length of the dendrites to
the soma. For a long time it was thought that postsynaptic
currents propagated passively and decrementally along
the dendrites: passively because dendrites do not generate
action potentials, the propagation of the signal depending
only on the cable properties of the dendrite; and decre-
mentally because the signal attenuates as it propagates,
owing to the leakage properties of the membrane. From
this it would be expected that depolarizations evoked by
distal excitatory synapses would be smaller in amplitude
at the soma and would have a longer risetime than depo-
larizations evoked by proximal synapses.
In fact, it seems that propagation is not always passive
and not always decremental. There may be at least two
types of propagation of postsynaptic currents through
dendrites:
• a passive and decremental propagation, which
implies an attenuation of distal postsynaptic
currents;
• a passive but only slightly decremental propagation,
which occurs where the cable properties of the
dendrite are very good and involve no attenuation,
or a weak attenuation, of distal postsynaptic currents.
These two alternatives are treated in Sections 13.1.2
and 13.1.3.
13.1.1 The complexity of synaptic organization
(Figure 13.1)
Presynaptic complexity
A presynaptic afferent axon gives off many axon ter-
minals (terminal boutons or ‘en passant’ terminals). In
this way, it generally establishes several synaptic con-
tacts with the postsynaptic neuron. In addition, the post-
synaptic neuron receives synapses coming from many
other presynaptic axons. It is thus possible to distinguish
several levels of complexity in postsynaptic potentials:
• the postsynaptic potential evoked in the absence
of presynaptic action potential (in the presence of
tetrodotoxin (TTX)) by the spontaneous fusion
of a synaptic vesicle with the presynaptic membrane:
miniature postsynaptic potential;
• the postsynaptic potential representing the sum
of postsynaptic potentials generated by synaptic
boutons coming from the same presynaptic axon:
unitary postsynaptic potential;
• the postsynaptic potential representing the sum of all
the postsynaptic potentials generated at all the active
synaptic boutons: composite postsynaptic potential.
FIGURE 13.1 Schematic of a neuron and some of its afferents.
Afferent fibers establish synaptic contacts on spines and dendritic
branches which are situated at different distances from the soma of the
postsynaptic neuron. When these afferents are activated, the depolar-
izing or hyperpolarizing postsynaptic currents are conducted towards
the soma and initial segment of the axon. It is at this level that the
response of the postsynaptic neuron is generated. The response is then
conducted along the axon and its collateral branches.

3. 13.1 Propagation of excitatory and inhibitory postsynaptic potentials through the dendritic arborization 287
III. Somato-Dendritic Processing and Plasticity of Postsynaptic Potentials
Postsynaptic complexity
Differentdendriticpostsynapticregions(spines,branch-
es and main trunks) are not equivalent. The diameter of
dendritictrunksisgreaterthanthatofbranches,particular-
ly distal branches. Thus, different dendritic compartments
have different resistances (note that R = ρl/s, ρ being the
resistivity, l the length and s the cross-section of the den-
drite). This means that spines with a neck, or a very small
diameter pedicle, have a high resistance. Consequently,
synaptic currents generated at different points do not give
the same potential change: for the same inward current I,
the amplitude of the resulting postsynaptic depolarization
(VEPSP) will be greater for the dendritic regions where the
resistance rm = 1/gm is large (VEPSP = IEPSP/gm).
Complexities of the propagation of postsynaptic
action potentials
Postsynaptic potentials (EPSPs and IPSPs) propagate
along the dendrites to the action potential initiation zone,
which is generally situated in the initial region of the axon
(initial segment). Depending on the cable properties of the
dendrites, the postsynaptic potentials can change their char-
acteristics (amplitude, risetime) during their propagation.
13.1.2 Passive decremental propagation
of postsynaptic potentials
‘Decremental’ means that the postsynaptic potentials
attenuate as they propagate. This implies that the post-
synaptic potentials are not regenerated at each point
along the dendrites, as is the action potential as it trav-
els along the axon. This passive propagation depends
on the cable properties of the dendrite. In order to es-
timate quantitatively the modifications of postsynaptic
potentials in the course of their conduction, a theoretical
model of the passive properties of membrane potential
changes was first established by Wilfred Rall from data
obtained on the squid giant axon. Thus, a postsynaptic
potential conducted with decrement (i) reduces in am-
plitude, and (ii) has a risetime (rt) which gets longer as it
is propagated along the dendrites (Figure 13.2).
FIGURE 13.2 Theoretical model of decremental conduction of excitatory postsynaptic potentials (EPSP) along dendrites. (a) Four EPSPs
numbered 1 to 4 are generated at the instant t between t = 0 and t = 0.25 ms (black bar in simulation diagram on left), at different sites within the
dendritic tree (schematic drawing on right). At the site of generation, these EPSPs are identical in amplitude and duration. After conduction along
the dendrites, their shapes are different (theoretical recordings at the level of the soma, simulation diagram on left). It can be observed that the
further away the site of generation of the EPSP (case 4), the smaller is its amplitude and the longer is its risetime (rt) when it arrives at the level of
the soma (compare the theoretical recordings 1 to 4). (b) Theoretical model of the linear summation of EPSP (see text for explanation). From Rall
W (1977) Handbook of Physiology, vol. 1, part 1, Bethesda, MA: American Physiological Society, with permission.

4. 288 13. Somato-dendritic processing of postsynaptic potentials I: Passive properties of dendrites
III. Somato-Dendritic Processing and Plasticity of Postsynaptic Potentials
The reduction in amplitude of the postsynaptic cur-
rent as it gets further from the generation site is due to the
fact that the current flows not only longitudinally along
the dendrite but also transversely across the channels
that are open in the dendritic membrane potential. This
‘leak’ of ions towards the extracellular medium results in
a reduction in the postsynaptic current and a consequent
reduction in the amplitude of the postsynaptic potential.
Thus, the fewer the number of channels open in the den-
dritic membrane, the higher will be the value of rm, the
better will be the cable properties of the dendrite and
the less will be the reduction in amplitude of postsynap-
tic potentials of distal origin.
The increase in the risetime of the postsynaptic poten-
tials is due to the fact that part of the postsynaptic cur-
rent serves to charge the capacity of each unit of mem-
brane along the dendrite. The consequence of this is a
change in the time course of the postsynaptic current: as
it gets further from its point of generation, its risetime
becomes longer (it can also be said that the speed of ris-
ing becomes slower).
13.1.3 Passive and non-decremental propagation
of postsynaptic potentials
This type of propagation means that postsynaptic po-
tentials are conducted passively along the dendrites but,
because of the good cable properties of the dendritic ar-
borization, they are almost unattenuated as they propa-
gate. Thus, in the model of the synapse of Ia afferent fi-
bers with spinal motoneurons, it has been shown that the
unitary EPSPs evoked by the activity of afferent fibers
and recorded in the soma have very similar amplitudes
even though their risetimes may be different; i.e. when
they are generated at different distances from the soma.
This implies that, in this model, there must be local den-
dritic mechanisms that allow an almost non-attenuating
conduction of the distal postsynaptic potentials.
13.2 SUMMATION OF EXCITATORY
AND INHIBITORY POSTSYNAPTIC
POTENTIALS
13.2.1 Linear and non-linear summation
of excitatory postsynaptic potentials
In general, many excitatory synaptic afferents con-
verge on a single neuron. At each excitatory synapse that
is activated, there is an inward current of positive charges.
When the membrane potential is not held at a fixed value,
this inward current of positive charges depolarizes the
postsynaptic membrane: this is the postsynaptic poten-
tial, or EPSP (see, for example, the current clamp record-
ings of the synaptic response to glutamate in Chapter 10).
A unitary EPSP (meaning one caused by the activa-
tion of a single afferent fiber; Section 13.1.1) cannot trig-
ger action potentials. EPSPs generated in isolation are
too small in amplitude to depolarize the membrane of
the initial segment to the threshold potential for the
opening of voltage-sensitive Na+
channels. However, if
many EPSPs generated at different sites in the dendritic
arborization arrive more or less simultaneously at the
level of the initial segment, the probability that they will
generate action potentials becomes much greater. This is
due to the fact that the EPSPs summate.
Linear summation of excitatory postsynaptic
potentials
The term ‘linear summation’ means that the compos-
ite EPSP (see Section 13.1.1) resulting from the activity
of several excitatory synapses has an amplitude that is
equal to the geometric sum of the different EPSPs contrib-
uting to it. This is true when the EPSPs are generated at
sites that are sufficiently far or isolated from one another
to avoid interactions between them (on different dendrit-
ic branches, or on different dendritic spines, for instance).
A postsynaptic neuron generally receives many excit-
atory synapses at different points on its somato-dendritic
arborization (see Figures 13.1 and 13.2a). These EPSPs
summate as they propagate, in a temporo-spatial manner.
To grasp this phenomenon, it must be understood that
the EPSPs generated at different sites in the dendritic
arborization and conducted to the initial segment of the
axon can arrive spread out in time. The offset between the
EPSPs will depend on the distances between the genera-
tion sites and on the respective times at which they were
generated. The examples demonstrated here are based
on theoretical calculations of the cable properties of den-
drites. These data give a qualitative understanding of the
phenomenon of summation but do not constitute a real
experimental demonstration.
Let us consider the example of four EPSPs of the same
amplitude, generated at different sites in the dendritic ar-
borization, at times such that their arrivals at the initial seg-
ment are offset in time. Figure 13.2b shows the ‘composite
EPSP’ obtained in two cases of arrival sequences. In the case
1 → 2 → 3 → 4, the four EPSPs are generated at the same
time t; but since some are generated at more distal sites,
their arrivals at the initial segment are staggered, the most
proximal arriving first and the most distal arriving last. In
the case 4 → 3 → 2 → 1, the most distal EPSPs are generated
well before the proximal EPSPs, so that the distal EPSPs ar-
rive before the proximal EPSPs. The theoretical results show
that in the first case, in which the proximal EPSPs occur first
and are followed by the more distal EPSPs, the ‘composite
EPSP’ has a short latency, a long duration and a small am-
plitude; while in the second case, in which the distal EPSPs
arrive before the proximal EPSPs, the ‘composite EPSP’ has
a long latency and a large amplitude (Figure 13.2b).

5. 13.2 Summation of excitatory and inhibitory postsynaptic potentials 289
III. Somato-Dendritic Processing and Plasticity of Postsynaptic Potentials
The following experiment supports theoretical cal-
culations. Simultaneous whole-cell recordings are per-
formed from three interconnected pyramidal cells. Two
of these neurons are presynaptic to the third. The com-
posite EPSP evoked when the two presynaptic cells are
stimulated simultaneously is equal to the linear sum of
the unitary EPSPs evoked when each cell is stimulated
separately. Subsequent morphological reconstruction
of the pre- and postsynaptic neurons are performed to
confirm that the presynaptic terminals are on different
branches of the postsynaptic cell’s basal dendrites and
hence probably electrotonically distant from each other.
Non-linear summation of excitatory postsynaptic
potentials
The term ‘non-linear summation’ means that the
‘composite EPSP’ has an amplitude that is not equal to
the geometric sum of the different EPSPs contributing
to it. This occurs, for instance, when two EPSPs are gen-
erated at the same site or at sites that are close.
Let us take the example of two excitatory synapses
whose neurotransmitter is glutamate and which are
situated close together on the same dendritic segment
(Figure 13.3), supposing that the membrane potential of
the dendritic segment is Vm. When synapse 1 is active
alone, EPSP1 is recorded, due to the excitatory postsyn-
aptic current I1, such that I1 = gcations (Vm − Ecations), whose
amplitude is VEPSP1 = I1/gm, where gm is the membrane
conductance (Figure 13.3a). When synapse 2 is active
alone, EPSP2 is recorded at level 2, due to the postsyn-
aptic current I2, such that I2 = gcations (Vm − Ecations), whose
amplitude is VEPSP2 = I2/gm (Figure 13.3b). If we suppose
that when the two EPSPs are generated separately, VEP-
SP1 = VEPSP2, what is the amplitude of the ‘composite EPSP’
when the two synapses are active at the same time?
When synapse 1 is activated first, EPSP1 is recorded in
the postsynaptic element and will be conducted passive-
ly to neighboring regions (Figure 13.3a). At time t + ∆t,
EPSP1 arrives at the postsynaptic element 2. The mem-
brane of the postsynaptic element 2 is then at a potential
Vm9 which is more positive than Vm (Figure 13.3c). If at
this moment (t + ∆t) synapse 2 is active, the postsynaptic
current I29 will be smaller than if it had taken place inde-
pendently from I1 because the electrochemical gradient
of Na+
and Ca2+
ions is reduced. I29 = gcations(Vm9 − Ecations)
and I29 < I2 because (Vm9 − Ecations) < (Vm − Ecations). The
‘composite EPSP’ will have an amplitude less than the
geometric sum EPSP1 + EPSP2 (Figure 13.3c).
This is also the case when a single excitatory synapse
is activated repetitively by the arrival of high-frequency
presynaptic action potentials. When an excitatory post-
synaptic current is generated before the preceding current
has ended, it has a smaller amplitude because the post-
synaptic membrane is depolarized. Thus, during high-
frequency activation, successive excitatory postsynaptic
potentials have amplitudes that are smaller and smaller.
FIGURE 13.3 Non-linear summation of excitatory postsynaptic potentials. Suppose that there are two excitatory synapses situated close
together on the same dendritic segment. (a) When afferent 1 is activated at time t, a depolarization of the postsynaptic membrane 1 is recorded at
time t (EPSP1 alone). This depolarization propagates in the two directions away from 1. (b) When afferent 2 is activated, at time t + ∆t, a depolar-
ization of the postsynaptic membrane 2 is recorded (EPSP2 alone). (c) When the two afferents 1 and 2 are activated as before, but together, one at
time t and the other at time t + ∆t, a depolarization of the postsynaptic membrane 2 (OEPSP) is recorded at time t + ∆t, which does not correspond
to the geometric sum EPSP1 alone + EPSP2 alone, since EPSP29 has an amplitude which is smaller than EPSP2 (see text for explanation).

6. 290 13. Somato-dendritic processing of postsynaptic potentials I: Passive properties of dendrites
III. Somato-Dendritic Processing and Plasticity of Postsynaptic Potentials
13.2.2 Linear and non-linear summation
of inhibitory postsynaptic potentials
When inhibitory synapses are active they cause, in the
postsynaptic membrane, an outward postsynaptic cur-
rent of positive charges (carried by K+
ions) or an inward
current of negative charges (carried by Cl−
ions) which
hyperpolarizes the membrane: this is the inhibitory post-
synaptic potential, or IPSP.
Linear summation of IPSPs is symmetrically the same
as linear summation of EPSPs. Non-linear summation of
IPSPs is symmetrically the same as non-linear summa-
tion of EPSPs.
13.2.3 The integration of excitatory and
inhibitory postsynaptic potentials partly determines
the configuration of the postsynaptic discharge
In order for an action potential to be triggered at the ini-
tial segment, the membrane of the initial segment must be
depolarized to the threshold potential for the opening of
voltage-sensitive Na+
channels. It is also necessary for this
depolarization to have a relatively rapid risetime so that the
Na+
channels do not inactivate during the depolarization.
The characteristics of depolarization of the initial segment
(amplitude, duration, risetime) result partly from the sum-
mation of excitatory and inhibitory postsynaptic potentials.
FIGURE 13.4 Integration of excitatory (EPSP) and inhibitory (IPSP) postsynaptic potentials. (a) Suppose that on a dendritic tree, there are
glutaminergic excitatory synapses which are situated distally, and GABAB-type inhibitory synapses which are situated proximally, and that all of
these are active at the same instant t. (b) If only the excitatory synapses are active, a depolarization, a composite EPSP (OEPSP) will be recorded at
the soma which corresponds to the linear and non-linear summation of all the different EPSPs (top trace). We will suppose that the OEPSP has an
amplitude that is sufficient to trigger an action potential (upper trace). If only the inhibitory synapses are active, a hyperpolarization, a composite
IPSP (OIPSP) will be recorded at the soma which corresponds to the linear and non-linear summation of all the different IPSPs (middle trace).
When all these different synapses are activated at the same time t, a depolarization preceded by a hyperpolarization, a composite PSP, will be
recorded at the soma, corresponding to the sum of the different synaptic potentials (OEPSP + OIPSP) (bottom trace). In this case, the amplitude of
the depolarization is no longer sufficient to trigger an action potential. (c) Electrical equivalent of the membrane at the level of the initial segment,
for an EPSP alone. (d) Electrical equivalent for the membrane when an EPSP and an IPSP summate. The currents IEPSP and IIPSP are opposite and
subtract from one another. By comparing with (c), it is observed that IEPSP in (c) is greater than IEPSP + IIPSP in (d), and ∆Vl > ∆V2.

7. 13.2 Summation of excitatory and inhibitory postsynaptic potentials 291
III. Somato-Dendritic Processing and Plasticity of Postsynaptic Potentials
Integration of depolarizing (excitatory)
postsynaptic potential with hyperpolarizing
(inhibitory) postsynaptic potential
A hyperpolarizing postsynaptic potential is due to a
current whose reversal potential is more negative than
the resting membrane potential of the cell. This type of
inhibition is generally due to the opening of K+
channels
(GABAB-type inhibition). Since the equilibrium potential
of K+
ions is more negative than the resting membrane
potential, the opening of K+
channels gives rise to an out-
ward current (an exit of positive charges) and to a hyper-
polarization of the membrane; i.e. an IPSP. If this IPSP is
concomitant with an EPSP, it will reduce the amplitude
of the EPSP. This type of summation of EPSP and IPSP is
summarized in Figure 13.4.
Integration of depolarizing (excitatory)
postsynaptic potential and silent (inhibitory)
postsynaptic potential
A silent postsynaptic potential is due to a current
whose reversal potential is close to the resting potential
of the cell. Generally, this is caused by a current of Cl−
ions through GABAA channels (see Chapter 9). When
the equilibrium potential of Cl−
ions is close to the mem-
brane resting potential, the opening of Cl−
channels does
not reveal a hyperpolarizing current at the resting poten-
tial (from which comes the term ‘silent’ for this inhibi-
tion). However, when the membrane is depolarized by
an EPSP, the inhibition is no longer silent, but becomes
hyperpolarizing. The result is the reduction or even the
complete suppression of the EPSP (Figure 13.5).
FIGURE 13.5 Role of silent inhibition. (a) This diagram shows two synapses, one glutamatergic with postsynaptic AMPA receptors (E1) and
the other GABAergic with GABAA postsynaptic receptors (I1), situated close to one another on the same dendritic segment, such that the inhibi-
tory synapse is closer to the soma than the excitatory synapse. (b) When the excitatory synapse is excited alone, an EPSP of ∆V1 in amplitude is
recorded (b1). When the inhibitory synapse is activated alone, no change in potential is recorded because Vm = ECl (b2). When both synapses are
activated, the EPSP which propagates towards the soma is reduced in amplitude (amplitude ∆V3), or even cancelled out. This type of inhibition is
selective because it only acts on excitatory synapses that are situated distally. (c) Electrical equivalent of the membrane at the dendritic segment.
If this is compared with Figure 13.4c, it can be seen that ∆V3 < ∆V1 because gm + gIPSP > gm.

8. 292 13. Somato-dendritic processing of postsynaptic potentials I: Passive properties of dendrites
III. Somato-Dendritic Processing and Plasticity of Postsynaptic Potentials
Integration of depolarizing (excitatory)
postsynaptic potential and depolarizing inhibitory
postsynaptic potential
A depolarizing inhibitory postsynaptic potential is
due to a synaptic current whose reversal potential is more
positive than the resting potential of the membrane but
more negative than the threshold for the opening of the
Na+
channels of the action potential. This is generally due
to the opening of Cl−
channels in cells in which the re-
versal potential for Cl−
ions is situated between the rest-
ing potential and the threshold potential for the opening
of the Na+
channels of the action potential. Thus, when
the membrane is at its resting potential, this Cl−
current
causes a slight depolarization of the membrane, but does
not trigger action potentials. When the membrane is de-
polarized (by an EPSP) above the inversion potential of
Cl−
ions, this current causes a hyperpolarization of the
membrane and an inhibition of the EPSP.
13.3 SUMMARY
Several types of inhibition appear over the length of
the somato-dendritic arborization and these limit the ef-
fect of excitatory synapses. The opening or non-opening
of the Na+
channels of the action potential and, in con-
sequence, the generation of action potentials which will
constitute the response of the postsynaptic neuron, are
the result of this summation of excitatory and inhibi-
tory postsynaptic potentials. However, the characteris-
tics of the response of the postsynaptic neuron are de-
termined not only by the amplitude and duration of the
depolarization of synaptic origin but also by the char-
acteristics of the membrane of the initial segment, also
known as ‘input–output’ characteristics.
Further reading
Buhl, E.H., Halasy, K., Somogyi, P., 1994. Diverse sources of
hippocampal unitary inhibitory postsynaptic potentials and the
number of release sites. Nature 368, 823–828.
Cauller, L.J., Connors B.W., 1992. Functions of very distal dendrites.
In: McKenna, T.M., Davis, J., Zornetzer, S.E. (Eds.), Single Neuron
Computation. Academic Press, New York.
Gulledge, A.T., Kampa, B.M., Stuart, G.J., 2005. Synaptic integration in
dendritic trees. J. Neurobiol. 64, 75–90.
Larkum, M.E., Launey, T., Dityatev, A., Lüscher, H.R., 1998.
Integration of excitatory postsynaptic potentials in dendrites of
motoneurons of rat spinal cord slice cultures. J. Neurophysiol. 80,
924–935.
Miles, R., Toth, K., Gulyas, A.I., Hajos, N., Freund, T.F., 1996.
Differences between somatic and dendritic inhibition in the
hippocampus. Neuron 16, 815–823.
Rall, W., 1977. Core conductor theory and cable properties of neurons.
In: Brookhart, J.M., Mountcastle, V.B., Kandel, E.R., Geiger,
S.R. (Eds.), Handbook of Physiology, vol. 1, part 1. American
Physiological Society, Bethesda, MD.
Redman, S.J., 1973. The attenuation of passively propagating dendritic
potentials in a motoneuron cable model. J. Physiol. 234, 637–664.
Reyes, A., 2001. Influence of dendritic conductances on the input-
output properties of neurons. Annu. Rev. Neurosci. 24, 653–675.
Shepherd, G.M., 1994. The significance of real neuroarchitectures
for neural network simulations. In: Schwartz, E.L. (Ed.),
Computational Neuroscience. Oxford University Press, New York.
Spruston, N., Johnston, D., 1992. Perforated patch clamp analysis of
the passive membrane properties of three classes of hippocampal
neurons. J. Neurophysiol. 67, 508–528.
Spruston, N., Jaffe, D.B., Johnston, D., 1994. Dendritic attenuation of
synaptic potentials and currents: the role of passive membrane
properties. Trends Neurosci. 17, 161–166.