Skip to main content

Advertisement

Log in

Versatile, robust, and efficient tractography with constrained higher-order tensor fODFs

  • Original Article
  • Published:
International Journal of Computer Assisted Radiology and Surgery Aims and scope Submit manuscript

Abstract

Purpose

Develop a multi-fiber tractography method that produces fast and robust results based on input data from a wide range of diffusion MRI protocols, including high angular resolution diffusion imaging, multi-shell imaging, and clinical diffusion spectrum imaging (DSI)

Methods

In a unified deconvolution framework for different types of diffusion MRI protocols, we represent fiber orientation distribution functions as higher-order tensors, which permits use of a novel positive definiteness constraint (H-psd) that makes estimation from noisy input more robust. The resulting directions are used for deterministic fiber tracking with branching.

Results

We quantify accuracy on simulated data, as well as condition numbers and computation times on clinical data. We qualitatively investigate the benefits when processing suboptimal data, and show direct comparisons to several state-of-the-art techniques.

Conclusion

The proposed method works faster than state-of-the-art approaches, achieves higher angular resolution on simulated data with known ground truth, and plausible results on clinical data. In addition to working with the same data as previous methods for multi-tissue deconvolution, it also supports DSI data.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Andersson JLR, Sotiropoulos SN (2016) An integrated approach to correction for off-resonance effects and subject movement in diffusion mr imaging. NeuroImage 125:1063–1078

    Article  PubMed  PubMed Central  Google Scholar 

  2. Ankele M, Lim LH, Groeschel S, Schultz T (2016) Fast and accurate multi-tissue deconvolution using SHORE and H-psd tensors. In: Proceedings of medical image analysis and computer-aided intervention (MICCAI) part III, LNCS, vol 9902. Springer, Berlin, pp 502–510

  3. Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44:625–632

    Article  CAS  PubMed  Google Scholar 

  4. Canales-Rodríguez EJ, Iturria-Medina Y, Alemán-Gómez Y, Melie-García L (2010) Deconvolution in diffusion spectrum imaging. NeuroImage 50:136–149

    Article  PubMed  Google Scholar 

  5. Chen Z, Tie Y, Olubiyi O, Zhang F, Mehrtash A, Rigolo L, Kahali P, Norton I, Pasternak O, Rathi Y, Golby AJ, O’Donnell LJ (2016) Corticospinal tract modeling for neurosurgical planning by tracking through regions of peritumoral edema and crossing fibers using two-tensor unscented kalman filter tractography. Int J Comput Assist Radiol Surg 11(8):1475–1486

    Article  PubMed  PubMed Central  Google Scholar 

  6. Cheng J, Deriche R, Jiang T, Shen D, Yap PT (2014) Non-negative spherical deconvolution (NNSD) for estimation of fiber orientation distribution function in single-/multi-shell diffusion MRI. NeuroImage 101:750–764

    Article  PubMed  Google Scholar 

  7. Christiaens D, Sunaert S, Suetens P, Maes F (2016) Convexity-constrained and nonnegativity-constrained spherical factorization in diffusion-weighted imaging. NeuroImage 146:507–517. doi:10.1016/j.neuroimage.2016.10.040

  8. Descoteaux M, Deriche R, Knösche TR, Anwander A (2009) Deterministic and probabilistic tractography based on complex fibre orientation distributions. IEEE Trans Med Imaging 28(2):269–286

    Article  PubMed  Google Scholar 

  9. Garyfallidis E, Brett M, Amirbekian B, Rokem A, Van Der Walt S, Descoteaux M, Nimmo-Smith I (2014) Dipy, a library for the analysis of diffusion MRI data. Front Neuroinform. 8(8). doi:10.3389/fninf.2014.00008

  10. Jeurissen B, Tournier JD, Dhollander T, Connelly A, Sijbers J (2014) Multi-tissue constrained spherical deconvolution for improved analysis of multi-shell diffusion MRI data. NeuroImage 103:411–426

    Article  PubMed  Google Scholar 

  11. Jiao F, Gur Y, Johnson CR, Joshi S (2011) Detection of crossing white matter fibers with high-order tensors and rank-\(k\) decompositions. In: Székely G, Hahn HK (eds) IPMI, LNCS, vol 6801, pp 538–549

  12. Jones DK, Knösche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. NeuroImage 73:239–254

    Article  PubMed  Google Scholar 

  13. Knutsson H, Westin CF (2013) Tensor metrics and charged containers for 3d q-space sample distribution. In: Mori K, Sakuma I, Sato Y, Barillot C, Navab N (eds) Proceedings of medical image computing and computer-assisted intervention (MICCAI) part I, LNCS, vol 8149, Springer, Berlin, pp 679–686

  14. Malcolm JG, Michailovich O, Bouix S, Westin CF, Shenton ME, Rathi Y (2010) A filtered approach to neural tractography using the Watson directional function. Med Image Anal 14:58–69

    Article  PubMed  Google Scholar 

  15. Merlet SL, Deriche R (2013) Continuous diffusion signal, EAP and ODF estimation via compressive sensing in diffusion MRI. Med Image Anal 17:556–572

    Article  PubMed  Google Scholar 

  16. Mori S, Crain BJ, Chacko VP, van Zijl PCM (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45(2):265–269

    Article  CAS  PubMed  Google Scholar 

  17. Özarslan E, Mareci T (2003) Generalized diffusion tensor imaging and analytical relationships between diffusion tensor imaging and high angular resolution diffusion imaging. Magn Reson Med 50:955–965

    Article  PubMed  Google Scholar 

  18. Paquette M, Merlet S, Gilbert G, Deriche R, Descoteaux M (2015) Comparison of sampling strategies and sparsifying transforms to improve compressed sensing diffusion spectrum imaging. Magn Reson Med 73(1):401–416

    Article  PubMed  Google Scholar 

  19. Raffelt D, Tournier JD, Rose S, Ridgway GR, Henderson R, Crozier S, Salvado O, Connelly A (2012) Apparent fibre density: a novel measure for the analysis of diffusion-weighted magnetic resonance images. NeuroImage 59(4):3976–3994

    Article  PubMed  Google Scholar 

  20. Reisert M, Mader I, Anastasopoulos C, Weigel M, Schnell S, Kiselev V (2011) Global fiber reconstruction becomes practical. NeuroImage 54(2):955–962

    Article  PubMed  Google Scholar 

  21. Reznick B (1992) Sums of even powers of real linear forms. American Mathematical Society

  22. Schultz T, Fuster A, Ghosh A, Deriche R, Florack L, Lim LH (2014) Higher-order tensors in diffusion imaging. In: Westin CF, Vilanova A, Burgeth B (eds) Visualization and processing of tensors and higher order descriptors for multi-valued data. Springer, Berlin, pp 129–161

  23. Schultz T, Groeschel S (2013) Auto-calibrating spherical deconvolution based on ODF sparsity. In: Mori K, Sakuma I, Sato Y, Barillot C, Navab N (eds) Proceedings of medical image computing and computer-assisted intervention (MICCAI) part I, LNCS, vol 8149. Springer, Berlin, pp 663–670

  24. Schultz T, Seidel HP (2008) Estimating crossing fibers: a tensor decomposition approach. IEEE Trans Vis Comput Gr 14(6):1635–1642

    Article  Google Scholar 

  25. Tournier JD, Calamante F, Connelly A (2010) Improved probabilistic streamlines tractography by 2nd order integration over fiber orientation distributions. In: Proceedings of international society of magnetic resonance in medicine (ISMRM), p 1670

  26. Tournier JD, Calamante F, Connelly A (2007) Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. NeuroImage 35:1459–1472

    Article  PubMed  Google Scholar 

  27. Tournier JD, Calamante F, Connelly A (2012) MRtrix: diffusion tractography in crossing fiber regions. Int J Imaging Syst Technol 22(1):53–66

    Article  Google Scholar 

  28. Tournier JD, Calamante F, Gadian DG, Connelly A (2004) Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. NeuroImage 23:1176–1185

    Article  PubMed  Google Scholar 

  29. Vandenberghe L (2010) The CVXOPT linear and quadratic cone program solvers. Tech. rep., UCLA Electrical Engineering Department. http://www.seas.ucla.edu/~vandenbe/publications/coneprog.pdf

  30. Wedeen V, Wang R, Schmahmann J, Benner T, Tseng W, Dai G, Pandya D, Hagmann P, D’Arceuil H, de Crespigny A (2008) Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. NeuroImage 41(4):1267–1277

    Article  CAS  PubMed  Google Scholar 

  31. Wedeen VJ, Hagmann P, Tseng WYI, Reese TG, Weisskoff RM (2005) Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 54(6):1377–1386

    Article  PubMed  Google Scholar 

  32. Wedeen VJ, Rosene DL, Wang R, Dai G, Mortazavi F, Hagmann P, Kaas JH, Tseng WYI (2012) The geometric structure of the brain fiber pathways. Science 335(6076):1628–1634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Weldeselassie YT, Barmpoutis A, Atkins MS (2012) Symmetric positive semi-definite cartesian tensor fiber orientation distributions (CT-FOD). Med Image Anal 16(6):1121–1129

    Article  PubMed  Google Scholar 

  34. Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20(1):45–57

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the DFG under Grant SCHU 3040/1-1. LHL is supported by AFOSR FA9550-13-1-0133, DARPA D15AP00109, NSF IIS 1546413, DMS 1209136, and DMS 1057064.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas Schultz.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the local ethics committee. All volunteers gave their written informed consent for participation in the study.

Additional information

This work was supported by the DFG under Grant SCHU 3040/1-1. LHL is supported by AFOSR FA9550-13-1-0133, DARPA D15AP00109, NSF IIS 1546413, DMS 1209136, and DMS 1057064.

Appendix: Mathematical derivation of H-psd constraint

Appendix: Mathematical derivation of H-psd constraint

This appendix presents the formal definition of our H-psd constraint (Definition 4), based on a matrix representation H of higher-order tensor fODFs (Definition 3). According to Corollary 1, H is positive semidefinite if and only if the corresponding fODF can be decomposed into a nonnegative weighted sum of rank-1 terms, which correspond to single fiber compartments in our framework. This provides the theoretical justification of our H-psd constraint, whose practical effectiveness is demonstrated in the main part of the paper.

We represent fODFs as forms or symmetric tensors p of even degree \(d=4\) in \(n=3\) dimensions. In tensor notation:

$$\begin{aligned} p(\mathbf x ) = p(\underbrace{\mathbf{x , \dots , \mathbf x }}_{d}) = \sum _{i \in \{1,\dots ,n\}^d} p_{i_1,\dots ,i_d} \, x_{i_1} \dots x_{i_d}, \quad \mathbf x \in \mathbb {R}^n. \end{aligned}$$
(7)

We will call the set of these forms \(F_{n,d}\). Symmetry allows us to use a different, nonredundant indexing scheme

$$\begin{aligned} p(\mathbf x ) = \sum _{i \in I(n,d)} {d \atopwithdelims ()i} \, p_i \, x^i \end{aligned}$$
(8)

with multi-indices \(i \in I(n,d) = \{i \in {\mathbb {N}_0}^n | \sum _k i_k = d\}\), multinomial coefficients \({d \atopwithdelims ()i} = \frac{d!}{\prod i_k!}\) and monomial terms \(x^i = \prod _{k=1}^n (x_k)^{i_k}\).

Our constraint stems from the relations of three subsets of \(F_{n,d}\):

$$\begin{aligned} P_{n,d}&= \left\{ p \in F_{n,d} : p(\mathbf x ) \ge 0, \forall \, \mathbf x \in \mathbb {R}^n\right\} \nonumber \\&\qquad \text {``positive semidefinite''} \end{aligned}$$
(9)
$$\begin{aligned} \varSigma _{n,d}&= \left\{ p \in F_{n,d} : p(\mathbf x ) = \sum _k h_k(\mathbf x )^2\right\} \nonumber \\&\qquad \text {``sums of squares''} \end{aligned}$$
(10)
$$\begin{aligned} Q_{n,d}&= \left\{ p \in F_{n,d} : p(\mathbf x ) = \sum _k \langle \mathbf a _k, \mathbf x \rangle ^d\right\} \nonumber \\&\qquad \text {``sums of d-th powers''} \end{aligned}$$
(11)

Here, the \(h_k(\mathbf x )\) denote forms of degree d / 2, \(\mathbf {a}_k\) denote the individual vectors that define the rank-1 terms of a nonnegative decomposition.

As shown in [21], these three subsets obey

$$\begin{aligned} Q_{n,d} \subset \varSigma _{n,d} \subset P_{n,d}. \end{aligned}$$
(12)

These sets cannot be vector spaces, since if \(p \ne 0\) is positive, \(-p\) is not. So the concept of vector spaces has to be weakened:

Definition 1

A convex cone is a subset C of \(F_{n,d}\) that obeys:

  • \( p,q \in C \quad \Rightarrow \quad p+q \in C\)

  • \( p \in C, \lambda \ge 0 \quad \Rightarrow \quad \lambda p \in C\)

\(P_{n,d}\), \(\varSigma _{n,d}\) and \(Q_{n,d}\) are closed convex cones.

The definition of our constraint and its properties depend on the choice of a scalar product for forms.

Definition 2

A scalar product on \(F_{n,d}\) can be defined as

$$\begin{aligned}{}[p,q] = \sum _i {d \atopwithdelims ()i} \, p_i \, q_i. \end{aligned}$$
(13)

For \(Q_{n,d}\), this scalar product has a particularly simple form:

Lemma 1

For \(p = \sum _k \langle \mathbf a _k, \cdot \rangle ^d \in Q_{n,d}\) and \(q \in F_{n,d}\) we have

$$\begin{aligned}{}[q,p] = \sum _k q(\mathbf a _k). \end{aligned}$$
(14)

Proof

By the multinomial theorem:

$$\begin{aligned} \langle \mathbf a , \mathbf x \rangle ^d = \left( \sum _{i=1}^n a_i \, x_i \right) ^d = \sum _{i_1 + \dots + i_n = d} {d \atopwithdelims ()i} a^i \, x^i \end{aligned}$$
(15)

And so

$$\begin{aligned}{}[q,p]&= [q, \sum _k \langle \mathbf a _k, \cdot \rangle ^d] = \sum _k [q, \langle \mathbf a _k, \cdot \rangle ^d] \\&= \sum _k \sum _i {d \atopwithdelims ()i} q_i \cdot (a_k)^i = \sum _k q(\mathbf a _k). \end{aligned}$$

\(\square \)

Also note that \([\cdot ,\cdot ]\) corresponds to the usual scalar product for tensors and [pp] is the square of the Frobenius norm \(\Vert p\Vert _F\).

In order to derive a matrix representation, we want to reduce a form of even degree \(d=2s\) to \(d'=2\). For this, we need

$$\begin{aligned} L(\mathbf x ,t) = \sum _i x^i \, t_i \end{aligned}$$
(16)

with a vector of variables t indexed by \(i \in I(n,s)\). For fixed t, this is a \(F_{n,s}\) form in \(\mathbf x \). For fixed \(\mathbf x \), this is a linear form in t.

Definition 3

For \(p \in F_{n,2s}\), the Hankel form is the quadratic form

$$\begin{aligned} H_p(t) = [p, L^2(\cdot ,t)] = \sum _{i,j} p_{i+j} \, t_i \, t_{j} \, \in F_{|I(n,s)|,2}. \end{aligned}$$
(17)

We can put this into matrix form as \(H_p(t) = t^T H_p \, t\). For \(p \in F_{3,4}\), the matrix is

$$\begin{aligned} H_p = \begin{pmatrix} p_{xxxx} &{} p_{xxxy} &{} p_{xxxz} &{} p_{xxyy} &{} p_{xxyz} &{} p_{xxzz} \\ p_{xxxy} &{} p_{xxyy} &{} p_{xxyz} &{} p_{xyyy} &{} p_{xyyz} &{} p_{xyzz} \\ p_{xxxz} &{} p_{xxyz} &{} p_{xxzz} &{} p_{xyyz} &{} p_{xyzz} &{} p_{xzzz} \\ p_{xxyy} &{} p_{xyyy} &{} p_{xyyz} &{} p_{yyyy} &{} p_{yyyz} &{} p_{yyzz} \\ p_{xxyz} &{} p_{xyyz} &{} p_{xyzz} &{} p_{yyyz} &{} p_{yyzz} &{} p_{yzzz} \\ p_{xxzz} &{} p_{xyzz} &{} p_{xzzz} &{} p_{yyzz} &{} p_{yzzz} &{} p_{zzzz} \end{pmatrix}. \end{aligned}$$
(18)

Definition 4

A form p with positive semidefinite \(H_p\) will be called H-psd.

$$\begin{aligned} H_{n,d} = \{p \in F_{n,d} : H_p(t) \ge 0 \; \forall \, t\} \end{aligned}$$
(19)

The method we propose enforces the H-psd constraint on fODFs during deconvolution.

In the rest of this section, we will discuss some properties of the set \(H_{n,d}\) that are relevant to our method. The main tool will be duality:

Definition 5

The dual cone of a convex cone C is the set

$$\begin{aligned} C^\star = \{p \in F_{n,d} : [p,q] \ge 0, \; \forall \, q \in C \} \,. \end{aligned}$$
(20)

If C is a closed convex cone, then (see Reznick [21])

$$\begin{aligned} C^{\star \star } = C. \end{aligned}$$
(21)

Theorem 1

\(P_{n,d}\) and \(Q_{n,d}\) are dual to each other:

$$\begin{aligned} {Q_{n,d}}^\star = P_{n,d}, \qquad {P_{n,d}}^\star = Q_{n,d} \end{aligned}$$
(22)

Proof

$$\begin{aligned} p \in {Q_{n,d}}^\star \;&\Longleftrightarrow \; 0 \le [q,p] = [\sum _k \langle \mathbf a _k, \cdot \rangle ^d, p] \nonumber \\&\qquad = \sum _k p(\mathbf a _k), \quad \forall \, q \in Q_{n,d} \\&\Longleftrightarrow \; 0 \le p(\mathbf a ), \quad \forall \, \mathbf a \in \mathbb {R}^n \\&\Longleftrightarrow \; p \in P_{n,d} \end{aligned}$$

The second equation is a consequence of \({Q_{n,d}}^{\star \star } = Q_{n,d}\).

\(\square \)

In the special case of \((n,d)=(3,4)\), the H-psd constraint is equivalent to decomposability into rank-1 terms. This can be shown with the following two theorems:

Theorem 2

(Hilbert)

$$\begin{aligned} P_{n,d} = \varSigma _{n,d} \end{aligned}$$
(23)

if and only if \(n=2\) or \(d=2\) or \((n,d) = (3,4)\).

Theorem 3

$$\begin{aligned} {\varSigma _{n,d}}^\star = H_{n,d} \end{aligned}$$
(24)

Proof

Observe that \(t \mapsto L(x,t)\) is a bijection between vectors \(t\in \mathbb {R}^{|I(n,s)|}\) and forms in \(F_{n,s}\). So:

$$\begin{aligned} p \in {\varSigma _{n,d}}^\star \;&\Longleftrightarrow \; 0 \le [p, q] = [p, \sum _k h_k^2] \quad \forall \, q \in \varSigma _{n,d} \\&\Longleftrightarrow \; 0 \le [p, h^2] \quad \forall \, h \in F_{n,s} \\&\Longleftrightarrow \; 0 \le [p, L(\cdot , t)^2] = H_p(t) \quad \forall \, t \in \mathbb {R}^{|I(n,s)|} \end{aligned}$$

\(\square \)

A direct consequence for \((n,d)=(3,4)\) is:

Corollary 1

\(p \in F_{3,4}\) is a sum of fourth powers iff it is H-psd, since

$$\begin{aligned} Q_{3,4} = {P_{3,4}}^\star = {\varSigma _{3,4}}^\star = H_{3,4}. \end{aligned}$$
(25)

For higher degrees, the relation is weaker:

$$\begin{aligned} Q_{3,n} \subsetneq H_{3,n} \subset P_{3,n} \end{aligned}$$
(26)

Another property of the H matrix is that it can be used to estimate the number of fibers in an fODF.

Definition 6

The rank of \(p \in Q_{n,d}\) is the smallest integer \({\text {rank}}(p)=r\) for which \(\mathbf a _1,\dots ,\mathbf a _r \in \mathbb {R}^n\) can be found with

$$\begin{aligned} p = \sum _{k=1}^{r} \langle \mathbf a _k, \cdot \rangle ^d. \end{aligned}$$
(27)

For the cases in Hilbert’s Theorem 2, the ranks of p and \(H_p\) are equal as shown in theorem 4.6 in [21]. In general, \({\text {rank}}(p) \ge {\text {rank}}(H_p)\).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ankele, M., Lim, LH., Groeschel, S. et al. Versatile, robust, and efficient tractography with constrained higher-order tensor fODFs. Int J CARS 12, 1257–1270 (2017). https://doi.org/10.1007/s11548-017-1593-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11548-017-1593-6

Keywords

Navigation